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Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort Pierce, Florida 34949
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Abstract |
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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This pattern of tube growth creates two problems for the few species of serpulids that, in addition to producing larvae by sexual reproduction, reproduce asexually. Asexual reproduction is best known in members of the widely distributed genera Filograna and Salmacina (see Materials and Methods for comments on the systematics of these taxa), though it occurs in members of at least five other genera as well (Filogranella, Filogranula, Josephella, Rhodopsis, and Spiraserpula: H. ten Hove, Zoological Museum, Amsterdam, The Netherlands, pers. comm.; ten Hove, 1979; Nishi and Yamasu, 1992; Pillai and ten Hove, 1994). Adults of Filograna and Salmacina spp. reproduce asexually by paratomous fission, releasing a single budded offspring at a time from the posterior end (Malaquin, 1895; Faulkner, 1930; Cresp, 1964). A newly released bud is thus effectively sealed in a tube whose only opening is blocked by the parent worm. How do these asexually derived individuals gain access to the exterior environment to feed, grow, and reproduce? Once they have gained access to the exterior, how do they build their own tubes?
An important clue is that adults of Filograna and Salmacina spp. occur in conspecific aggregations of branching tubes. Though individual adults of these species are small, rarely exceeding 500 µm in diameter and a few millimeters in length, aggregations may be composed of hundreds or thousands of individuals and reach dimensions of tens of centimeters (ten Hove, 1979; Nishi and Nishihira, 1997). Observations of aggregation growth and form suggest that asexually derived individuals somehow form tubes that branch off from the tubes of their parents (Benham, 1927; Hanson, 1948). Benham (1927) suggested that new tubes branch from the mouths of parental tubes. This might obtain, for example, if a parent shared its tube opening with a bud while the latter began to build a new tube. In contrast, Hanson (1948) concluded that newly released buds bore holes in the parental tubes to gain access to the exterior and then build their own tubes starting from these newly created openings. Either of these hypotheses would account for both the escape of clonal offspring from the parental tubes and the formation of aggregations of branching tubes. Determining which, if either, is correct requires more detailed observations of the processes of asexual reproduction and tube growth.
In this paper I report the results of such observations on the serpulid Salmacina amphidentata. I show that each bud gains access to the exterior of the parental tube via an escape hatch built into the tube for it by the parent worm. It then uses the parental tube as a starting point for building its own tube. A survey of Filograna and Salmacina spp. from the Atlantic, Indian, and Pacific oceans suggests that this pattern of tube growth, among the most complex known in the serpulids, is widespread among members of these genera. These observations raise novel questions concerning the evolution of both asexual reproduction and tube formation in serpulids, as well as the signals that coordinate these two processes.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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Systematics of Filograna and Salmacina
I identify the Floridian specimens studied here as Salmacina amphidentata, but both the generic and specific names applied are tentative. Members of Filograna and Salmacina have been distinguished by the presence or absence, respectively, of opercula; because this trait may be variable even within species, Zibrowius (1968) transferred Salmacina spp. to the older genus Filograna. Despite this, some systematists continue to refer to operculate forms as Filograna spp. and inoperculate forms as Salmacina spp. (e.g., ten Hove and Wolf, 1984), a practice I continue here. The species-level systematics of these genera are also uncertain (Zibrowius, 1973; ten Hove and Wolf, 1984). Nine species of Salmacina have been described (ten Hove, pers. comm.), but most descriptions are based on only a few specimens from single localities, and the degree of variation in what are considered distinguishing traits has usually not been assessed (but see Gee, 1963; Nishi, 1992). Confident identification to species will only be possible following a revision of these taxa. The specimens I studied closely resembled Salmacina amphidentata from Jamaica (Jones, 1962). They differed from the description of that species only in their greater maximum number of chaetigers (33 vs. 25), greater variation in number of thoracic chaetigers (seven or eight, rarely six, vs. seven, rarely six), and larger size of thoracic and abdominal uncini. Voucher specimens have been deposited in the U.S. National Museum of Natural History (#186807).
Observations of asexual reproduction and tube growth
Aggregations of living worms were examined with a dissecting microscope soon after collection to study tube morphology and branching patterns. Detailed observations of asexual reproduction and tube growth were made on worms cultured in the laboratory. Cultures were initiated by chipping individual worms in their tubes from the substrates on which they were collected. I blotted tubes dry and attached them to numbered glass microscope slides with cyanoacrylate glue. Slides were held in open plastic slide boxes submerged in containers of vigorously aerated seawater (salinity 34 ppt) at 25°C. I changed the water in containers every other day, and after each water change added enough cells of Isochrysis and Nannochloris to color the water slightly. Worms grew rapidly under these conditions, adding new tube material at the anterior end and producing clonal offspring. I examined them daily with a dissecting microscope to study tube growth. New sections of tube typically grew prostrate, attached directly to the glass slides. Because these tubes were incomplete in cross-section, I could follow the events of asexual reproduction in individual worms by looking into tubes through the glass slides. Asexual reproductive stages were observed at higher magnifications by dissecting worms from their tubes and examining them with a compound microscope. I also used time-lapse video to observe tube growth more continuously in two individuals. The growing margins of tubes viewed through a dissecting microscope equipped with a color CCD video camera were recorded on a time-lapse recorder set to record one frame every 0.2 s.
Views of the external morphology of tubes and worms were obtained by scanning electron microscopy (SEM). Tubes recently collected from the field were prepared for SEM by first chipping portions of interest from the substratum. They were fixed for 10 min in 5% formalin in seawater, rinsed in distilled water, dehydrated in several changes of 100% ethanol, and air-dried. Worms to be prepared for SEM were removed from their tubes and relaxed in a mixture of 7.5% MgCl2 and seawater, then fixed in 5% formalin in seawater for 30 min, rinsed in seawater, and post-fixed in 1% osmium in seawater for 2–4 h. They were rinsed several times in distilled water, dehydrated in an ascending concentration series of ethanol solutions, and critical-point dried with CO2 as the transitional fluid. Specimens were mounted on stubs with adhesive carbon tabs (Ted Pella, Inc.) and sputter-coated with gold before being viewed with a JEOL 6400V microscope.
I sectioned several tubes in order to examine their internal structure, using modifications of methods suggested by K. Fauchald (National Museum of Natural History, Smithsonian Institution, Washington, DC) and K. Fitzhugh (Los Angeles County Museum of Natural History, Los Angeles, CA). Pieces of tubes recently collected from the field were prepared as for SEM, except that once dehydrated they were transferred through several changes of propylene oxide and embedded in PolyBed 812 resin (Polysciences Inc.). Excess polymerized resin was removed with a Buehler Isomet low-speed saw equipped with a diamond wafering blade, and trimmed blocks were glued to glass petrographic slides with five-minute epoxy resin. Blocks were then sectioned with the low-speed saw and polished to the desired level with a Buehler Ecomet 2 grinder-polisher. Finally, I stained the sectioned surface in a solution of hot azure II and methylene blue (each 0.5%, in 0.5% sodium borate: Richardson et al., 1960) for 1 min, rinsed with distilled water, air-dried, and covered the cut surface with immersion oil and a coverslip for photography.
Tube growth in Filograna and Salmacina spp. from other regions
I examined patterns of tube growth in aggregations of Filograna and Salmacina spp. from localities in the Atlantic, Indian, and Pacific oceans. Sources of material included the U.S. National Museum of Natural History and specimens in my own collections.
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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Posterior to the thorax is a short achaetigerous body region, and behind this is the abdomen. In the abdomen the positions of the chaetae are reversed relative to those of the thorax—here, the uncini are dorsal and elongate chaetae are ventral. This pattern of chaetal inversion is found in all serpulids, as well as in the related sabellariids and sabellids (Fitzhugh, 1989). The abdomen is variable in length, and is composed of from 5 to 25 chaetigerous segments. Finally, the terminal end of the abdomen is capped by the pygidium, which bears the anus.
Asexual reproduction and tube growth
Worms raised in the laboratory grew rapidly, adding to their tubes at rates of up to several millimeters a day. The process of normal tube growth in Salmacina amphidentata was similar to that described in other serpulids (e.g., Hedley, 1956, 1958; Neff, 1971). Worms added to the anterior margins of their tubes while they were actively feeding, with the radioles extended out of the tube opening and the three lobes of the collar folded back over the tube margin. The ventral collar lobe bore two lateral pores on the surface that was in contact with the tube margin (not shown); I assumed that these were the openings of the calcium-secreting glands, as in other serpulids (Hedley, 1956). Time-lapse video sequences revealed that calcareous material was slowly added to the tube margin underneath the collar flaps, resulting in an increase in tube length. Growth was not continuous, but resulted from bouts of feeding and tube deposition that lasted for a few minutes and were interrupted by retraction of the worms into their tubes for variable lengths of time.
In addition to adding to their tubes, worms raised in the laboratory reproduced asexually, with most adults releasing from one to four buds per month. (They did not reproduce sexually during this 6-month study, though a few aggregations collected from the field during this period contained sexually mature adults and larvae brooded in the parental tubes.) The events of asexual reproduction in Salmacina amphidentata were very similar to those described in other species of Filograna and Salmacina (e.g., Malaquin, 1895; Faulkner, 1930; Cresp, 1964). Briefly, the first overt sign of asexual reproduction in an adult worm was the appearance of a dense accumulation of bright orange granules in the coelomic cavities of a variable number (5–15) of its posteriormost abdominal segments. Soon after this accumulation of granules appeared, two dorsolateral groups of rudimentary radioles, four on each side, developed on the anteriormost abdominal segment that contained orange granules; these radioles marked the anterior end of the new bud (Fig. 2A, B). At this stage, radioles were simple unciliated cylinders and bore no pinnules. The rudiments of the thoracic membranes appeared at this time as well, as two small dorsolateral flaps of tissue posterior to the radioles (Fig. 2B). The demarcation between the body regions of the bud became evident soon after with the shedding of the originally adult abdominal chaetae in the first segment of the bud, and the sequential development (anterior to posterior) of three thoracic chaetigers from this segment. The first thoracic chaetiger bore only elongate chaetae dorsally. The next two thoracic chaetigers, which developed soon after the first, bore both dorsal elongate chaetae and ventral uncini. Posterior to these new thoracic chaetigers, the segments retained the abdominal configuration of chaetae present when the segments belonged to the adult (i.e., uncini were dorsal). During this time, the gut of the bud remained continuous with that of the adult, and algal cells ingested by the adult passed through the developing bud. Though I did not follow the timing of early events of asexual reproduction in detail, the period from the initial appearance of orange granules in the posterior of an adult to the stage illustrated in Figure 2 took no more than 4 days.
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1–3 µm: Fig. 3E) that lined the entire inner surface of the tube.
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Once the escape hatch was complete (12–18 h after it was started), the adult continued producing a normal cylindrical tube (Figs. 3C–E). During this time, the bud continued to develop. It added additional thoracic segments by transformation of the anteriormost abdominal segments, and added abdominal segments by typical annelid teloblastic growth (Malaquin, 1895; Faulkner, 1930; Cresp, 1964). The radioles elongated, developed pinnules, and became ciliated. In 18 budding events whose timing I followed carefully, the bud detached from the parent worm from 2 to 10 days (mean = 3.3) after formation of the escape hatch. The detached bud could move forward and backward in the parent’s tube, but it was unable to approach the main tube opening, which was blocked by the parent’s body. By this time, however, the parent had typically added 3–8 mm of new tube beyond the escape hatch, so this structure was accessible to the bud. From 1 to 7 days (mean = 2.5) after the bud had detached from the parent, the calcareous disc was pushed out of the escape hatch. I did not observe this process as it happened, so I do not know which worm (parent or bud) actually dislodged the disc. Soon after the disc was dislodged, the bud began to feed from the resulting opening. The disc often remained precariously attached to the hole for several weeks, presumably by the organic membrane that had originally held it in place (Fig. 4A).
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Once a bud had gained access to the exterior via the escape hatch, it constructed its own tube using the parental tube as a starting point (Fig. 4A, B). As the new tube emerged from the hole, it was initially directed upward at an angle of about 45 degrees from the parent’s tube, continuous with the peristome formed by the parent immediately prior to constructing the escape hatch (Fig. 4B), but it usually curved back down to the substratum rapidly. A new bud would often build a peristome and escape hatch in its new tube just a few hundred micrometers beyond its point of emergence from the parent’s tube. This new escape hatch was eventually used by the bud’s own asexually produced offspring 1 to 2 weeks later.
This growth pattern was seen several hundred times in laboratory-raised aggregations. In field-collected aggregations, events of asexual reproduction and tube growth were more difficult to follow, because the substrate was opaque, the aggregations were composed of dense masses of tubes, and tubes were partly covered with other encrusting organisms. Nevertheless, all stages of skeletal growth described above were seen regularly in aggregations collected from the field. Peristomes in tubes were almost always immediately followed by either escape hatches or tubes branching off. The junction between a parental tube and the tube of a bud was always located immediately distal to a peristome in the parental tube. On a few occasions, recently dislodged calcareous discs were seen at the junction between bud and parental tubes.
Tube growth in Filograna and Salmacina spp. from other regions
I examined aggregations of Filograna and Salmacina spp. from the Atlantic, Indian, and Pacific oceans in the collections of the U.S. National Museum of Natural History, and in my own collections (Table 1). In all of the aggregations I examined that had clearly visible branching tubes, branching patterns were as described above for Salmacina amphidentata. Side tubes always branched from parental tubes immediately distal to peristomes in the parental tube. Further, in three lots of preserved material from the Pacific ocean, I observed escape hatches identical in form to those described above.
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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It is remarkable that escape hatches in the tubes of Filograna and Salmacina spp. have not been described before, since asexual reproduction in these two genera has been the focus of detailed studies for well over a century (e.g., Huxley, 1855; Malaquin, 1895; Faulkner, 1930; Vannini and Ranzoli, 1954; Cresp, 1964; Nishi and Nishihira, 1994). In part, this may be because most of these workers focused their attention specifically on the morphology of developing buds, and not on the consequences of posterior budding for clonal offspring. Still, the questions of how buds might escape parental tubes and subsequently form their own tubes have been asked regularly over the past 75 years (Benham, 1927; Hanson, 1948; ten Hove, 1979; Nishi, 1992; ten Hove and van den Hurk, 1993).
The observations reported here also show clearly how the clonal offspring of Salmacina amphidentata, and at least some other Filograna and Salmacina spp., are retained near parent worms and contribute to the growth of aggregations of branching tubes. It should be noted that aggregations of Filograna and Salmacina spp. are not necessarily composed only of the genetically identical offspring of a single founder individual. Recruitment of planktonic larvae may contribute substantially to their growth (Nishi et al., 1996; Nishi and Nishihira, 1997). The branching tubes characteristic of aggregations of Filograna and Salmacina spp., however, are undoubtedly the consequence of repeated bouts of asexual reproduction. Many species of serpulids that do not reproduce asexually also form aggregations (ten Hove and van den Hurk, 1993), but these do not contain branching tubes.
Mechanisms and timing of escape hatch formation in Salmacina amphidentata
Though the escape hatches formed by Salmacina amphidentata are among the most complex tube structures known from the serpulids, the actual mechanism of their formation does not seem to have required great modifications of the routine processes of tube growth. The ability to carefully control where calcareous tube material is deposited around the margin of the tube, which permits S. amphidentata to build escape hatches, is widespread in serpulids. Many species, for example, deposit more material at some locations around the tube margin than at others, resulting in the formation of sculptural elements like keels or spines (e.g., Pomatoceros triqueter: Hedley, 1958; Filogranula gracilis (as Omphalopoma): Zibrowius, 1968; Spiraserpula spp.: Pillai and ten Hove, 1994). A few species form even more complex structures such as brood chambers for developing embryos (Ben-Eliahu and ten Hove, 1989; Nishi, 1993). Adults of S. amphidentata avoid depositing any calcareous tube material at all in the narrow gaps between the calcareous disc and the rest of the tube, while depositing it elsewhere along the tube margin. Such precise control over the location of deposition may be mediated by two processes. First, the slurry of calcareous crystals in a fluid organic matrix may be deposited directly at the correct sites on the tube margin by the pair of calcium-secreting glands on the ventral lobe of the collar, with the adult rotating in the tube to position the gland openings correctly. However, in each of the two episodes of escape hatch formation I observed in detail by time-lapse video, the adult worm rotated in its tube infrequently. Further, for most of the time spent building hatches, the openings of calcium-secreting glands were approximately adjacent to the gaps between the calcareous disc and the rest of the tube, exactly where no calcareous tube material was deposited. A more plausible possibility is that muscular movements of the collar mold the slurry of tube material into the correct positions on the tube margin. I did not observe such movements, but would expect them to be subtle and difficult to see at the low magnifications used in this study. The slurry of tube material is not molded onto the tube margin by the action of cilia on the collar, as its relevant surfaces lack cilia (not shown).
In Salmacina amphidentata, the calcareous discs of the escape hatches were supported in place by a thin organic membrane (Fig. 3E). This organic layer lined the inner surface of the entire tube. Though it is rarely mentioned in accounts of tube structure or growth, a similar "coating membrane" has been found lining the tubes of at least five other species of serpulids (Muzii, 1968; Pernet, pers. obs.), and is probably an integral component of the tube in all species of serpulids. This is presumably the material that the chaetae of serpulids interact with during routine movement up and down the tube, and also during anchoring when a predator attempts to pull the worm from the tube (e.g., Merz and Woodin, 2000). Two observations suggest that the coating membrane is deposited prior to or at the same time as the calcareous tube material. First, during the process of escape hatch formation, Filograna and Salmacina spp. construct a calcareous disc that is discontinuous with the rest of the calcareous tube. As noted earlier, however, it appears that the growth of calcareous tubes in all serpulids requires a pre-existing tube margin onto which new calcareous material can be added. During the deposition of calcareous discs, it seems likely that such a pre-existing tube margin is present in the form of a coating membrane. Second, the calcareous disc is supported in place by the coating membrane; it seems likely that this is true throughout its construction. That the coating membrane has been found in all serpulids that have been carefully examined (Muzii, 1968; Pernet, pers. obs.) and that it appears to be deposited prior to or simultaneously with the calcareous portion of the tube suggest that it plays an important and rarely considered role in tube formation. It may also be important in considerations of the evolution of the calcareous tube, a defining feature of the serpulids (Rouse, 2000).
The close temporal coordination of events in asexual reproduction and tube growth in Salmacina amphidentata suggests the possibility of signaling pathways between buds and parents. Only after a developing bud had reached a certain stage (with unbranched radioles, 0–3 thoracic segments, and rudimentary thoracic membranes) did the parent worm begin to form an escape hatch. Adults never built escape hatches unless they were in the midst of a budding cycle. What stimulates the parent worm to alter its pattern of tube deposition at this particular stage in bud development? It is possible that bud and escape hatch formation are part of a single developmental pathway in adult worms, such that once asexual reproduction is initiated, escape hatch formation several days later is inevitable. Alternatively, once a bud reaches a certain stage, it may somehow signal to the adult that it is an appropriate time to form an escape hatch. For example, buds at the stage shown in Figure 2 may already be producing their own hormonal products, perhaps involved in controlling such processes as the transformation of former adult abdominal segments into thoracic segments for the bud. Adult worms, which are still attached to the buds at this stage, might use such signals as a cue to alter their patterns of tube deposition. Endocrine substances produced in the prostomium (or in other parts of the anterior end) are well known as signals controlling the timing of asexual reproduction and changes in chaetal morphology in other polychaetes (e.g., Schroeder, 1967; Franke and Pfannenstiel, 1984). A test of this hypothesis might involve implanting the prostomium of a developing bud into the body of a non-budding adult, and examining the effects on tube growth.
Once buds have detached from the parent, they are free to move forward and backward in the parental tube. Within a few days, however, they must gain access to the outside via the escape hatch. I did not determine which worm actually dislodged the calcareous disc from the escape hatch, though it seems likely that the bud does this rather than the parent, which has usually grown well beyond the escape hatch by this time. Buds may identify the site of the escape hatch by simply moving around and testing the tube walls until they find a weak spot. Dislodging the calcareous disc presumably does not require much force, as it is held in place only by a very thin coating membrane.
I did not measure rates of asexual reproduction, or how these might be related to rates of tube growth. In laboratory cultures, both the frequency of asexual reproduction and the rate of tube growth appeared to vary within and among clones, resulting in great variation in the distance between side branches from parental tubes. Many factors, both environmental (food levels, temperature, water flow) and genetic, might affect these parameters, as has been described in other clonal organisms (e.g., Sebens, 1980; Keen and Gong, 1989). Understanding the determinants of rates of asexual reproduction and tube growth in Filograna and Salmacina spp. is of particular interest since these parameters should strongly affect the eventual form of clonal aggregations. In nature, aggregations are quite variable in form.
Distribution and evolution of escape hatches in asexually reproducing serpulids
Some Filograna and Salmacina spp. from the Atlantic, Indian, and Pacific oceans form escape hatches for their clonal offspring (Table 1). In three lots of relatively recently preserved material, escape hatches identical in form to those described above in Salmacina amphidentata were present. In the remaining six lots of material I examined, which had been in preservative for 18–107 years, branching patterns of tubes were identical to those described above, but no intact escape hatches were found. The absence of intact escape hatches in this older material is not too surprising, even if escape hatches were present at the time of collection. The tubes of these species are delicate and are often damaged during collection and handling. It is also likely that they are gradually dissolved during storage, unless preservatives are well buffered. Escape hatches in particular are prone to damage or dislodgement, as the organic membrane that supports calcareous discs in the tube is extremely thin (Fig. 3E). These comparative data suggest that the formation of escape hatches for clonal offspring is widespread in members of Filograna and Salmacina.
Asexual reproduction is also known from several other genera of serpulids (Filogranella, Filogranula, Josephella, Rhodopsis, and Spiraserpula). Members of these genera that reproduce asexually do so by posterior budding, as in Filograna and Salmacina spp. (ten Hove, 1979; Ben-Eliahu and ten Hove, 1989; Nishi, 1992; Pillai and ten Hove, 1994). Their clonal offspring should also face the dual problems of escaping from the parental tubes and starting to build their own tubes. How they solve these problems is not known. Aggregations of branching tubes similar to those of Filograna and Salmacina spp., suggesting some mechanism of reaching the exterior of the parental tube but not dispersing from it, are reported in members of three of these genera (Filogranella, Josephella, and Spiraserpula: ten Hove, pers. comm.; George, 1974; Pillai and ten Hove, 1994).
A few members of a closely related family of tube-dwelling polychaetes, the Sabellidae, also reproduce asexually by posterior budding (Knight-Jones and Bowden, 1984). Sabellid tubes are typically constructed of secreted organic compounds and sediment particles, and are not calcified. How the clonal offspring of sabellids escape the parental tubes is not known. Adults of several species are apparently capable of boring holes in their own tubes (Fitzsimmons, 1965), and it is possible that buds are able to do this as well. Once buds have gained access to the exterior of parental tubes, they may be free to disperse far from their parents before building new tubes, as many sabellids are able to build tubes de novo throughout their lives (Fitzsimmons, 1965; Lewis, 1968).
In serpulids, asexual reproduction by posterior budding is only profitable if buds have some way of gaining access to the exterior of the parent’s tube (such as escape hatches), but it is difficult to imagine how escape hatches might have evolved in the absence of asexual reproduction. One scenario for the evolution of both of these traits (which seem to be tightly correlated in extant species of Filograna and Salmacina, at least) involves the initial evolution of posterior budding. Tubes of serpulids—especially the very thin tubes characteristic of species that have small maximum body sizes (Nishi, 1993)—are easily damaged by chance biological or physical insults, and buds may have originally used such fortuitous openings to gain access to the exterior of parental tubes. Adult worms that secreted generally weaker skeletons, or skeletons with weak points, would have had more consistent success in fledging clonal offspring, though this might have been balanced by greater vulnerability to predators. Selection might then eventually lead to adults that built extremely weak points—escape hatches—into their tubes to ensure that buds would find exits. This is obviously speculative. However, this scenario might be tested with comparative data on living clonal serpulids examined in the context of a well-supported phylogeny. Neither sort of data is yet available. Such an analysis might reveal persistent and informative variation in the mechanisms buds use to gain access to the exterior of parental tubes.
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Acknowledgments |
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Footnotes |
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Literature Cited |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionLiterature Cited |
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