Spontaneous generation of bilateral symmetry in the paired claws and closer muscles of adult snapping shrimps
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1 Development 100, (1987) Printed in Great Britain The Company of Biologists Limited Spontaneous generation of bilateral symmetry in the paired claws and closer muscles of adult snapping shrimps JOANNE PEARCE and C. K. GOVIND Life Sciences Division, Scarborough Campus, University of Toronto, 1265 Military Trail, Scarborough, Ontario, Canada MIC 1A4 Summary Adult snapping shrimps Alpheus heterochelis (Say) have paired asymmetric claws consisting of a major or snapper claw and a minor or pincer claw. An unusual condition of bilateral symmetry consisting of paired snapper claws arose spontaneously in several snapping shrimps by transformation of the pincer to a snapper in the presence of an existing contralateral snapper claw. Transformation in the external morphology and fibre composition of the closer muscle was completed within two intermoult periods in the majority of cases where true symmetry was achieved and once established became permanent. Thus snapping shrimps, which are by nature solitary, when continually exposed to each other in the laboratory may transform their pincer to a snapper without any trauma to the existing snapper claw. Key words: muscle, claw, asymmetry, shrimp. Introduction Crustaceans such as homarid lobsters and alpheid shrimps, have bilaterally asymmetric claws consisting of an enlarged and elaborate major claw and a smaller, less elaborate minor claw. Occasionally, however, individuals are found with bilaterally symmetric claws either of the major or minor type; the former type being more rare than the latter. For example in wild populations of lobster Homarus americanus (Herrick, 1911; Emmel, 1908) and snapping shrimp Synalpheus longicarpus (Darby, 1934) the overwhelming majority (>99 %) possess paired asymmetric claws with an approximately equal distribution of handedness, while a small fraction have paired symmetric claws of the minor (<0-2 %) or major (<0-04 %) type. In snapping shrimps a reversal in claw asymmetry is possible throughout adult life (Przibram, 1901). Reversal occurs when the major, or snapper, claw is removed and the existing minor, or pincer, claw transforms into a major, while a new minor claw regenerates at the site of the original major. A symmetrical condition of either paired major, paired minor or paired intermediate-type claws, has been experimentally produced in the past (Wilson, 1903; Darby, 1934; Mellon & Stephens, 1978), but the fibre composition of the closer muscles in these unusual individuals has not been determined. Hence the question of whether there is true symmetry especially between paired major claws in snapping shrimps remains in abeyance. We describe for the first time the fibre composition of the closer muscles in paired snapper claws in shrimps displaying a rare condition of claw symmetry arising spontaneously from the normal asymmetric condition. Materials and methods Adult snapping shrimps, Alpheus heterochelis (Say), of both sexes were collected in beds of oyster shells exposed at low tide near Beaufort, North Carolina by W. D. Kirby-Smith and shipped to Toronto. The animals were sexed by examining the small pincer claw; males display a lateral expansion of the outer surface of the dactyl, which is conspicuously fringed with setae, while females possess a slender, biramous claw. The animals were held in individual compartments in 251 aquaria which were partitioned into 12 units with fibre glass screening and filled with artificial sea water (Instant Ocean, ph7-7). In this manner, life histories of each individual animal were monitored. The shrimps were fed once a day on a varied diet of frozen squid, smelt and commercially prepared trout food. They were held at room temperature which varied from 20 to 23 C and under these conditions the intermoult period lengthened from 18 days initially to days with extended captivity. The animals were
2 58 /. Pearce and C. K. Govind checked twice daily to monitor moulting and cast-off exoskeletons were removed immediately and photographed using a stereodissecting microscope in order to record changes in external claw morphology. The fibre composition of the claw closer muscles was determined using routine histochemical techniques for myofibrillar adenosine triphosphatase (ATPase) activity (Ogonowski & Lang, 1979). The animals were induced to autotomize their claws which were then frozen and serially cross sectioned in a cryostat. Cross sections of the claws were processed histochemically and photographed. The percent composition of fast and slow fibres was calculated by determining the relative cross-sectional surface areas of the two fibre types in selected regions of the muscle (Govind & Pearce, 1985). In the present report, the term pristine is utilized to denote the composition of the closer muscle in an animal that had been observed to undergo a minimum of two moults in the laboratory without changing claw configuration. Results External morphology of paired claws The first thoracic chelipeds of the snapping shrimp, Alpheus heterochelis, are markedly asymmetric consisting of a large major, or snapper, claw and a slender minor, or pincer, claw. The degree of claw specialization is illustrated in Fig. 1A by a female shrimp with a left snapper and a right pincer. Cross sections through the midregion of these claws (Fig. 1A, upper row) shows a uniform composition of all slow fibres in the closer muscle of the snapper claw, while the closer muscle in the pincer claw has a central band of fast fibres sandwiched by slow fibres. Over a period of several months in our laboratory, 5 animals out of 70 i.e. 7 % developed the unusual condition of bilateral symmetry by elaborating a second snapper claw in place of the pincer, while still maintaining an intact pristine snapper claw on the contralateral side. One of these unusual animals with paired snapper claws is shown in Fig. IB; also shown are cross sections of the pristine and new snapper claw, with all slow fibres in their closer muscles. The pristine snapper appears on the left while the new snapper is seen on the right side of the animal. A sixth animal, a male, also differentiated a second claw but of an intermediate type (Fig. 1C) displaying characteristics of both pincer and snapper claws. This claw on the right side of the animal lacks the robustness of the pristine contralateral snapper visible on the left. Cross sections of the pristine snapper show the typical staining pattern of all slow fibres in the closer muscle. However the intermediate-type claw has retained a central band of fast fibres typical of the male pincer closer muscle. The life histories of these six animals is presented in Table 1 and discussed below. The five individuals that developed paired snapper claws had for the previous one (PM10, PM11), two (SB 4, SB 6), or five moults (HI 8), possessed a normal pincer and snapper claw (Fig. 1A). While maintaining a completely functional snapper claw, the contralateral pincer claw transformed over the next two moults into a snapper claw. After the first transforming moult the new snapper typically displays many of the characteristic features of the pristine snapper claw in its external morphology. Exoskeletons from the claws of these animals show the elaboration of a hammer or plunger on the inner surface of the dactyl, with a reciprocal socket in the pollex (Fig. 2C,D,E,G). The dactyl broadens laterally and develops a pronounced curvature of its outer surface while the distal area of the propus develops an accentuated transverse groove. The degree of morphological change at this stage varies as illustrated by the claw in Fig. 2F, which failed to elaborate the hammer. As well, the male pincer claw (Fig. 2B) has a modified outer expansion of the dactyl, which is fringed with setae, and a less elaborate version of this secondary sexual characteristic is retained in the transforming claw (Fig. 2G). During the second intermoult period, transformation is essentially complete (Fig. 2H) although the new snapper is much smaller than its pristine counterpart. With succeeding moults, the snapper continues to hypertrophy and elaborate its form as seen in the series depicting the same claw after the first, second and fourth moults (Fig. 2E,H,I). Thus the change in external morphology of the transforming claw is similar to that which occurs during normal reversal of claw asymmetry, triggered by removal of the snapper (Przibram, 1901; Wilson, 1903; Darby, 1934, 1935; Stephens & Mellon, 1979a). Once established, the paired snapper condition is permanent as seen by the fact that PM11, moulted five times with no apparent sign of reversal. On the other hand, when both snapper claws were autotomized in SB 4, the shrimp regenerated paired asymmetric claws in the original configuration of left snapper and right pincer (Table 1). Thus the paired snapper condition does not persist following claw loss. Finally in one individual (PM9) the pincer-tosnapper transformation in terms of its external morphology did not progress beyond what was achieved in the first transforming moult period. This animal is shown in Fig. 1C, after it had completed three consecutive moults with an intermediate claw on the right side. The cast-off exoskeleton of this claw (Fig. 2J) displays a plunger and socket on the dactyl and pollex respectively, but does not show a deep
3 Claw muscle symmetry 1A 59 > Fig. 1. Different configurations of paired claws in adult snapping shrimps (lower row) and a representative cross section of these claws (upper row) showing fibre composition of the closer muscles stained for myofibrillar ATPase activity; dark-staining fast fibres and light-staining slow fibres. (A) Normal asymmetry of paired claws and closer muscles consisting of a snapper claw (left) with 100 % slow fibres and a pincer claw (right) with a band of fast fibres flanked by slow. (B) Unusual condition of symmetry consisting of pristine (left) and newly transformed (right) snapper claws, both with 100% slow fibres in their closer muscles. (C) Unusual condition of partial symmetry consisting of pristine snapper claw (left) with 100 % slow fibres and intermediate claw (right) with central fast fibre band flanked by slow. Magnification of animals x2-5 and of claw cross sections xl2. transverse groove or hypertrophy of the propus characteristic of a snapper. The animal was allowed to moult one more time for a total of four intermoult periods before both claws were removed and prepared for muscle examination. The transformed snapper claw in its external morphology represents an 'intermediate' form, exhibiting characteristics of both claw types. Fibre composition of paired closer muscles Several previous studies have characterized the fibre composition of the closer muscle in the paired asymmetric claws of Alpheus (Stephens & Mellon, I979a,b; O'Connor, Stephens & Leferovich, 1982; Govind, Mearow & Wong, 1986). The pristine snapper closer muscle is composed entirely of slow fibres, while the pincer closer muscle displays a central band of fast fibres flanked by slow fibres. In the closer muscle of shrimps with paired snapper claws we find both muscles to be composed of 100 % slow fibres when examined three moults after the claws became symmetric as in SB 6. When examined part way through the second and third intermoult cycle as in SB 4 and HI 8 respectively, the closer muscle of the pristine snapper displayed 100 % slow fibres (Fig. IB) whereas the newly transformed snapper muscle in the contralateral claw was composed almost entirely of slow fibres, except for the presence of a few fast fibres in the proximal region of the claw (Fig. 3, lower row, arrows). Just beyond this region, but still in the
4 60 J. Pearce and C. K. Govind Table 1. Configuration of paired right (R) and left (L) claws into snapper (S) and pincer (P) types in the intermoult periods before and after the development of the symmetric (paired snapper claw) condition from a previously asymmetric (paired pincer and snapper claw) condition in adult snapping shrimps, Alpheus heterochelis (Say) Identity of animal Number and duration (in days) of intermoults in asymmetric condition 1 1 Number and duration (in days) of intermoults in symmetric condition PM 10 (?) (30) (27) PM 11 SB 4* SB 6* HI 8* PM9* (14) (19) (25) (27) (34) (9) (11) (37) -/RP (21) (22) (29) (8) (18) LP/- (41) (18) (34) (23) (24) (22) (22) (23/18) (36) (16) (27) (26) (7) (14) (7) (23) (45) (27/21) (23) For each animal read successive moults from left to right. * Animals in which closer muscles were examined histochemically. proximal to middle area of the muscle, is a small space where the fast fibres had been located. As it previously has been shown that normal transformation of pincer claw to snapper involves the selective degeneration of fast fibres in the closer muscle (Mearow & Govind, 1985, 1986; Quigley & Mellon, 1986) the few proximal fibres are the sole remnants of a degenerative process which has eliminated the central band of fast fibres. Beyond this area in the central and distal regions of the claw, the closer muscle is composed entirely of slow muscle. Finally, a case of incomplete transformation of the closer muscle to the snapper condition was seen in PM 9 in which the claws were examined well into the fourth intermoult. The left pristine snapper claw displayed 100% slow fibres, typical of this muscle. The right newly transformed claw (Fig. 3, upper row), however, showed a central band of fast fibres comprising 18 % of the muscle mass in the region where the closer muscle has its largest cross-sectional area. This band of fast fibres extends bilaterally from the tendon in the proximal and middle half of the muscle, but unilaterally in the distal area, similar to a typical male pincer closer muscle in all respects. Modification of the distal region of the claw, i.e. elaboration of a hammer and socket, is therefore not indicative of muscle composition but rather it is hypertrophy of the propus and formation of an accentuated transverse groove which is more associated with a corresponding transformation of the closer muscle to 100 % slow fibres. Discussion The transformation of a pincer to snapper claw is usually triggered by the loss of the existing snapper. Wefindsuch transformations to occur in the presence of an intact snapper thus producing shrimps with paired snapper claws. In such animals claw symmetry is seen not only in the external morphology but also in the fibre composition of the closer muscle which is made up of 100 % slow fibres. Once such claw symmetry is established it appears to be permanent providing claw loss does not occur. Darby (1934) had two animals undergo three successive moults without losing this symmetrical condition and we had one go well into its fifth intermoult period without displaying any sign of reversal. However in the one case where both snapper claws were removed at the same time, the animal regenerated a snapper in the position of the pristine snapper and a normal pincer on the contralateral side. This suggests that the pristine snapper side may have retained some advantage over the contralateral side because when paired asymmetric (pincer and snapper) claws are removed simultaneously, they regenerate in their original configuration (Przibram, 1901; Wilson, 1903; Darby, 1934). Since wild shrimps with paired snapper claws are rare e.g. 2 out of 5000 or 0-04% in a population of Synalpheus longicarpis (Darby, 1934), the occurrence of these animals suggests that the symmetrical condition may simply represent an extreme case of normal variation within a population. In contrast in our laboratory we find a much higher incidence of
5 Claw muscle symmetry C (SB 4) 61 Dactyl - Plunger A (SB 6) J (PM 9) ^ & Fig. 2. Transformation of pristine female (A) and male (B) pincer claw into snapper type in the first, (C-G) second (H) and fourth (I) intermoult period. An intermediate type^(snapper) claw is shown in J. Principal features of a snapper claw are labelled in the line drawing. All of the transforming claws are from shrimps listed in Table 1 and are identified as such (in brackets). X4-5. shrimps (Alpheus heterochelis) with paired snapper claws i.e. 5 out of 70 or 7%, and this finding warrants an explanation. Claw symmetry has been produced in captive shrimps by various manipulations. Thus by removing first the pincer and at varying intervals afterwards, the snapper, Darby (1934) produced a small number of shrimps (14 out of 196) with paired symmetrical claws of which only about a third (4 out of 14) were of the snapper type; the remainder were of the pincer type. Elevation of the temperature, however, increased to 80% the number of double snappers amongst shrimps with symmetrical claws (Darby, 1935). Other ways for producing paired snapper claws have involved crushing the nerve to the snapper claw (Mellon & Stephens, 1978) or cooling the entire claw (Mellon & Cox, 1985). None of these treatments were applied to our snapping shrimps nor were they subjected to any violent and or long-term fluctuations in temperature or sustain any injury to their claws. Yet within 2 weeks to 4 months of being held in our laboratory during which time they moulted one to four times, they spontaneously transformed their pincer claw into a snapper in the presence of an intact contralateral snapper claw. Therefore transformation from an asymmetrical to symmetrical condition can be activated without any trauma or stress being applied specifically to the snapper claw. This raises the distinct possibility that our methods for holding snapping shrimps were stressful and therefore much more conducive to generating double snapper claws (7 % occurrence) than those in other laboratories. For example neither Darby (1934,1935) nor Mellon & Stephens (1978) reported the spontaneous generation of paired snapper claws in their control shrimps. In both laboratories, the animals were held in individual containers and thus completely isolated from their neighbours. In the wild, some conspecific encounters prevail even though these shrimps live in individual burrows and not communally. In our laboratory the animals were continually exposed to each other as they were held in
6 62 /. Pearce and C. K. Govind Fig. 3. Cross sections through proximal (A,B), middle (C), and distal (D) regions of the claw showing the closer muscle in all sections and the small dorsally situated opener muscle in the distal region. The frozen sections stained for myofibrillar ATPase activity in a snapper claw (lower row) from animal SB 4 on the second intermoult following transformation show a few remaining, darkly stained fast fibres (arrow) in the proximal region and a characteristic empty space (arrow) replacing the fast fibres in the proximomiddle area of the muscle. An intermediate type claw (upper row) from animal PM9 shows a central band of fast fibres flanked by slow. xl5. a communal tank and separated from each other by fibre glass screens. Such continual exposure to conspecific neighbours in otherwise solitary-living animals may have stressed some of them sufficiently to trigger claw transformation. What signals are imparted during such exposure to initiate claw transformation remains to be elucidated. We thank G. A. Lnenicka for helpful comments and criticism of the manuscript. Financial support was provided by the Natural Sciences and Engineering Research Council and the Muscular Dystrophy Association of Canada. References H. H. (1934). The mechanisms of asymmetry in the Alpheidae. Carnegie Inst. Wash. Publ. No. 435, DARBY, H. H. (1935). The mechanism of chela differentiation in the Crustacea. Carnegie Inst. Wash. 29, EMMEL, V. E. (1908). The experimental control of asymmetry at different stages in the development of the lobster. /. exp. Zool. 5, DARBY, GOVIND, C. K. & PEARCE, J. (1985). Enhanced reappearance of fast fibers in regenerating crayfish claw closer muscles. Devi Biol. 107, GOVIND, C. K., MEAROW, K. M. & WONG, A. (1986). Regeneration of fiber types in paired asymmetric closer muscles of the snapping shrimp, Alpheus heterochelis. J. exp. Biol. 123, HERRICK, F. H. (1911). Natural history of the American lobster. U.S. Bur. Fish. 29, MEAROW, K. M. & GOVIND, C. K. (1985). Muscle transformation in snapping shrimps: evidence for fiber degeneration. Soc. Neurosci. Abstr. 11, 920. MEAROW, K. M. & GOVIND, C. K. (1986). Selective degeneration of fast muscle during claw transformation in snapping shrimps. Devi Biol. 118, MELLON, DE F. JR & Cox, G. (1985). Low temperature reversible nerve block initiates claw transformation in Alpheid shrimps. Soc. Neurosci. Abstr. 11, 920. MELLON, DE F. JR & STEPHENS, P. J. (1978). Limb morphology and function are transformed by contralateral nerve section in snapping shrimps. Nature, Lond. 272, O'CONNOR, K., STEPHENS, P. J. & LEFOROVICH, J. M. (1982). Regional distribution of muscle fiber types in the asymmetric claws of Californian snapping shrimp. Biol. Bull. mar. biol. Lab. Woods Hole 163,
7 Claw muscle symmetry 63 OGONOWSKI, M. M. & LANG, F. (1979). Histochemical evidence for enzyme differences in crustacean fast and slow muscle. J. exp. Zool. 207, PRZIBRAM, H. (1901). Experimentelle Studien uber Regeneration. Wilhelm Roux Arch. EntwickMech. 11, QUIGLEY, M. M. & MELLON, DE F. JR (1986). Myofiber death plays a role in determining fiber type composition in the claw closer muscles of the snapping shrimp, Alpheus heterochelis. J. exp. Zool. 239, STEPHENS, P. J. & MELLON, DE F. JR (1979a). Modification of structure and synaptic physiology in transformed shrimp muscle. J. comp. Physiol. 132, STEPHENS, P. J. & MELLON, DE F. JR (1979b). Morphology and synaptic physiology of the main closer muscle in regenerating claws of Alpheus. J. comp. Physiol. 134, WILSON, E. B. (1903). Notes on the reversal of asymmetry in the regeneration of the chelae in Alpheus heterochelis. Biol. Bull. mar. biol. Lab. Woods Hole 4, {Accepted 19 January 1987)
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