Rhd

Figure 6 Summary of the muscles and stretch receptors in the telson of crayfish (Procambarus, Astacidea), mud shrimp (Upogebia, Thallasinidea), squat lobster (Munida, Galatheidae), albuneid sand crab (Blepharipoda), and hippid sand crab (Emerita). In crayfish and mud shrimp, uropod movements independent of the telson are severely limited by the recessed joint, the linkages between the proximal uropod musculature and the musculature of the sixth abdominal segment and telson (see Figure 5b; Paul etal., 1985; Paul, 1991), and the overlapping neural control of uropod and abdominal-telson movements (Larimer and Kennedy, 1969; Dumont and Wine, 1987). The sequential changes in the muscles that preceded the advent of hippid sand crabs' new mode of swimming with the uropods began with the shift of their combined action from axial flexion to uropod control when the AT muscle was lost and a new proprioceptor, which senses elevation of the uropod, appeared; these changes continued with the evolution of a muscle that inserts dorsally on the uropod (RS) in albuneid sand crabs, in which RS is too small to have any biomechanical action on the uropod. Finally, the shift in the insertion of the remaining axial flexor muscle (PTF) to the uropod and hypertrophy of the pair of antagonists, PTU and RS (see Figure 5), completely freed the hippid uropods from the axial neuromusculature. At the same time, a different telson-uropod stretch receptor replaced the original telson-uropod stretch receptor present in tailflipping anomalans. Muscles: AT, anterior telson; ATU, anterior telson-uropod; LTU, lateral telson-uropod; PTF, posterior telson flexor; PTU, posterior telson-uropod (PS, uropod power-stroke muscle in Hippidae); RS, uropod return stroke; VTF, ventral telson flexor. Data from Dumont and Wine (1987), Paul (1972, 1981b), Maitland etal. (1982), Paul etal. (1985), and Paul and Wilson (1994).

of motoneurons in the sixth abdominal ganglion revealed in silver-intensified backfills from their axons. a1 (right side) The three uropod RS motoneurons in E. analoga (left side, the two uropod PS (PTU) motoneurons); a2, the RS motoneurons in B. occidentals (white arrow to small medial soma in comparable relative position to its larger homologue in E. analoga). The intermingling of RS and uropod rotator motoneurons in sand crabs' sixth abdominal ganglion (not shown) and the similar positions and morphologies of the rotator motoneurons in sand crabs and crayfish may be evidence of the derivation of the RS neuromusculature from the sixth segment's uropod rotator neuromusculature (Paul, 1981b; Vidal Gadea et al, 2003). b, The PTF motoneurons in A6 backfilled from the left side in E. analoga (b1) and the right side in B. occidentalis (b2); see Dumont and Wine, 1987 for their homologues in crayfish. Maximum width of ganglia: E. analoga, 1 mm; B. occidentals, 0.35 mm.

muscle; Paul et al., 1985) inserts directly opposite (ventral to the pivot point) the insertion of the RS muscle, whereas its smaller synergist (posterior tel-son flexor (PTF) homologue) inserts more medially. These muscles have homologues with different mechanical actions in crayfish (Figures 5 and 6, and Section 1.07.3.2.2 below).

Did the unique joint and constellation of muscular elements needed to swim with the uropods evolve together as a massive developmental transformation in the tailfan? Tracing backward the evolutionary history of hippids (Figure 2), starting with relatives most closely resembling hippids and moving to those more similar to crayfish in morphology and behavior, uncovers in reverse order the major evolutionary transitions on the way to the appearance of uropod beating. Comparative analysis of anomalan species that display less modified locomotion and tailfans than those of hippid crabs revealed that the uropod RS muscle is a new muscle that appeared prior to the split of the two sand crab families. Transformation of ancestral decapod neuromusculature began even earlier. I will briefly describe these events in reverse order of their occurrence.

1.07.3.2.1 New muscle, new motoneurons The

RS muscle homologue in spiny sand crabs, which tailflip and retain telson flexor and telson-uropod muscles in their ancestral positions (see below), is so small and inconspicuous that it was overlooked until an anomalous tiny branch from the nerve innervating the uropod remoter muscles in the sixth abdominal segment was traced (Paul, 1981b). This tiny branch turns posterior into the telson to end on what appeared to be folds of arthrodial membrane in the anterolateral corner of the telson. These folds turned out to be a few short muscle fibers converging to an attachment on the dorsal arthrodial membrane of the uropod joint, a position corresponding precisely to that of the massive RS muscle of hippid crabs; this muscle has no counterpart in crayfish or other decapods (Figure 5). The hypothesis of homology of these vastly different-sized muscles is predicated on the assumption that a spiny sand crab's homologue of the RS muscle is innervated by three motoneurons having central positions and morphologies similar to those of the three RS motoneurons of mole crabs, and this proves to be the case. Although the RS motoneurons are vastly different in size, reflecting the size difference of the muscles innervated, their positions in the ganglion and the branching patterns of their neurites are very similar, despite the different overall shapes of this ganglion in the two sand crabs (Figure 7). The few, short muscle fibers of the albuneid RS muscle could have no mechanical action on the uropod, nor do they appear capable of even stiffening the joint. Their appearance in sand crabs that tailflip was presumably the result of an ontogenetic error in the common ancestor of hippids and albuneids that, while serving no function, had no detrimental effect and became fixed in the lineage and a prea-daptation for uropod swimming.

1.07.3.2.2 Altered (and conserved) functions of conserved neuromusculature While the relative sizes of homologous muscles in mole crabs and spiny sand crabs differ, there is only one qualitative (functional) difference that distinguishes their tail-fan neuromusculature. The insertion of the PTF muscle in hippids has been switched to the ventralmedial propodite, making it a limb muscle rather than the terminal member of the axial flexor musculature (Paul, 1981b; Paul et al., 1985; Dumont and Wine, 1987). Thus, in contrast to the recent origin of the uropod RS muscle, the PS musculature turns out to have heterogeneous derivations from separate components of ancestral tailfan muscles. Interestingly, the latter muscles assist in the PS phase (flexion) of tailflipping (Paul, 1981a, 1981b). That is, retained muscles that are PS synergists in tailflipping species became the PS muscles for uropod beating in Hippidae. This discovery was important, because it implies that qualitative changes in the central neural circuitry for swimming need not have been substantial in the transition from tailflipping to swimming with the uropods. In hippids, changes in the development of the tailfan brought together ancestrally disparate components that serve different mechanical actions in other species, but retained the ancestral association of PS (and recovery stroke, i.e., extension) neuromusculature. The conversion of decapod PTF muscle to a uropod PS synergist (Figures 5 and 6) would have removed the last constraint against uropod movement independent of the body axis, an essential step for evolution of hip-pids' mode of swimming with the uropods. Although recent molecular data have been interpreted to suggest a basal position of hippids within the Anomala (Haye et al., 2002), the combined morphological, physiological, behavioral, and ecological data support the contrary view that hippids are more derived than albuneids, as shown in Figure 2. The small size of the RS muscle in albuneids, therefore, is not the result of reduction of a larger muscle, as would be implied by placement of Hippidae at the base of the Anomala. A basal position of the Hippidae in the Anomala would mean that several reversals in transformation of neuromuscular elements would have had to occur. However, spiking telson-uropod stretch receptors (TUSR) (see Section 1.07.4) could have arisen once, even if sister group status of Galatheidae and Albuneidae were supported.

1.07.3.3 Ontogeny and Evolution of Neuromusculature

The development of neuromusculature in arthropods starts with the muscle fiber pioneers, which are meso-dermal cells that extend between attachment points of future muscles and, hence, determine the orientations and biomechanical actions of muscles (Ho et al., 1983; Steffens et al., 1995; Halpern, 1997). Later, the growth cones of motor axons exiting the central nervous system seek out the correct target muscle head or heads to innervate. The conversion of the axial PTF muscle to a limb muscle (PTFh in Figure 5a) described above probably arose by the wayward positioning of one or more muscle pioneers.

Muscles with multiple heads and new muscles are thought to originate by division of ancestrally unitary muscles, presumably by duplication of muscle pioneers (Ho et al. 1983; Halpern, 1997). One head can continue to serve the basic function, while the other(s) are less constrained functionally and may acquire new biomechanical and/or behavioral roles in response to selective pressure (Friel and Wainwright, 1997; Antonsen and Paul, 2000; Paul et al., 2002). This process may have given rise to the uropod RS muscle in sand crabs: its dorsal position in the telson and insertion adjacent to the complex tendon of the uropod rotator musculature in abdominal segment 6 (Figure 5) suggest that the RS muscle might have evolved by the wayward positioning of a rotator muscle fiber pioneer to place its axial attachment within the telson. Originally a triply innervated single head, as in albuneid sand crabs, this new muscle would have subsequently divided (or duplicated) to produce the four heads of the large uropod RS muscle in hippid sand crabs (Figures 5 and 7).

1.07.3.4 Intermediates between Sand Crab and Crayfish Tailfans

Stepping further down the hippid phylogenetic tree brings us to the Galatheidae (squat lobsters) (Figure 2). Apart from the absence of the uropod RS muscle from galatheids, the tailfan neuromusculature of squat lobsters and albuneid sand crabs is very similar (Figures 5 and 6). Squat lobsters, however, walk on the surface rather than locomote through substrate. (The major neurobehavioral adaptations in control of thoracic appendages and intersegmental coordination that enable sand crabs to dig through sand are described in Section 1.07.2.3.) Did loss of an ancient tailfan muscle precipitate alterations in the decapod tailfan and evolution of Anomala?

Preceding the transformations described above (and others) was the demise of the only telson muscle that has no anterior segmental homologue in decapods or any malacostracan, the AT muscle described above (Dumont and Wine, 1987; Paul and Macmillan, 1997). The large area of the inner telson surface vacated was then filled by the spread of the ATU muscle fibers, which in species with the AT muscle attach to the dorsal telson via a slender tendon (Figure 5). The discovery that the similarly positioned and oriented anomalan ATU muscle and crayfish's AT muscle are not homologues (Figure 5) opened the way to solving the puzzle of how the telson musculatures in these two groups were related (Paul et al., 1985). None of the anatomical literature on hermit crabs (Paguroidea) illustrates a muscle in the appropriate position (although a modified AT muscle could perhaps have been useful in gripping the inner whorl of gastropod shells with the uropod). If the AT muscle is indeed absent from hermit crabs, then its loss might have triggered the evolutionary modifications of the tail for which the Anomala are famous.

1.07.4 Did Loss of an Ancient Tailfan Muscle Precipitate Alterations in the Decapod Tailfan and Origin of the Anomala?

1.07.4.1 Identifying Neural Homologies in Divergent Species

Neuroblasts generally do not migrate from their birthplace during the embryonic development of the central nervous system in arthropods (Harzsch, 2003). Neurons with somata in similar positions relative to other landmarks in different species are, therefore, likely to be homologous (Figure 5). Motoneurons are more easily identified functionally and described morphologically than interneurons, because of the ease of applying the backfilling technique. Homologous motoneurons in turn serve as landmarks for comparing other neurons, as well as architectural features such as axonal tracts, commissures, and neuropil areas (Figure 8; Paul, 1989, 1991; Strausfeld, 1998; Loesel et al., 2002; Mulloney et al., 2003). Conserved central neural architecture of the tailfan ganglion provides the backdrop against which the new RS motoneurons were discovered in hippids, and from which corresponding (homologous) motoneurons were postulated and found in albuneids (above). Their possible derivation is addressed in Section 1.07.3.3. The RS motoneurons were not the only new neurons essential for swimming with the uropods.

1.07.4.2 Joints with Wide Freedom of Movement Require Proprioceptors to Keep Them in Line

Sensory feedback from stretch receptors and other internal proprioceptors, which detect changed position or tension between body parts, is used to sustain strong adaptive movements during locomotion (Pearson and Ramirez, 1997; Hooper and DiCaprio, 2004). On basic principles, one would predict that any joint as flexible as that of hippids' uropod articulation with abdominal segment 6 would display one or more stretch receptors, and this is the case. Hippids posses a TUSR that is exquisitely sensitive to remotion and rotation movements

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