Muscles of the Male - Part I

General Information -Development of the male muscle system - Diagonal muscles -Longitudinal muscles -Muscles of the Male Part II -Back to Contents

General Information

The muscle system of the male differs from that of the hermaphrodite primarily in its complement of sex muscles, derived from the M lineage. The adult male has 41 M-derived sex muscles consisting of 7 morphologically distinct types. None of these muscles are present in the hermaphrodite and so they are male-specific muscles. These muscles are distributed through the posterior half of the animal and function in various aspects of male mating behavior or copulation (MaleMusFIG1A, 1B, 2 ; Sulston and Horvitz, 1977; Sulston et al., 1980). Indeed, several sex muscles are directly associated with structures and tissues of the male copulatory apparatus such as the spicules and the gubernaculum. Surprisingly, males in which M has been ablated can execute most of the initial steps of mating (backing, turning, vulval location; Sulston, J.E., WBG 7(2):22), although their execution is significantly poorer than in wild type (see Loer and Kenyon, 1993). The spicules in such ablated animals do not function. Thus some male-specific muscles are essential for mating (e.g. the spicule muscles) while others appear to enhance the animal's ability adopt certain postures required during mating.

In addition to the sex muscles, a few embryonically-derived muscles that are present in both males and hermaphrodites (sphincter, anal depressor and body wall muscles) express different characteristics in the male and are employed in mating behavior or copulation (MaleMusFIG1B, underlined labels; Sulston and Horvitz, 1977; Sulston et al., 1980; Sulston et al., 1983).

 

With the exception of the longitudinal muscles, the (M-derived) sex muscles of the male generally conform to the non-striated class of muscle types (see MESODERMAL ORGANS, Part I - Hermaphrodite Handbook for a description of muscle types and MESODERMAL ORGANS, PART III - Hermaphrodite Handbook for hermaphrodite non-striated muscles). In contrast to striated muscles (e.g. body wall muscles), non-striated muscles contain a single or only a few sarcomeres (contractile units) and attach to cuticle only at their ends (denoted by red arrows in chapter figures; for organization of attachment sites see CutFIG9A - CUTICLE - Hermaphrodite Handbook; MusFIG38- MESODERMAL ORGANS, Part II - Hermaphrodite Handbook). The cuticle acts as an exoskeleton for muscle contraction to work against. In the male the cuticle may be body wall cuticle, as in the hermaphrodite, or a male-specific cuticle such as the spicules or the gubernaculum (MaleMusTABLE1). Certain subsets of muscles in the male are also connected to each other via attachment plaques (MaleMusTABLE1;denoted by yellow arrows in chapter figures). These muscle::muscle connections share some molecules in common with cuticle::muscle connections (see MESODERMAL ORGANS, Part II - Hermaphrodite Handbook). While the bulk of contractile force is likely to be transmitted to cuticle, muscle::muscle connections may transmit some pulling force between interconnected muscles, enhancing their ability to function as a unit (for example the spicule protactors and anal depressor muscles). Also like muscles elsewhere in the body, the male sex muscles have muscle arms and these are often the sites for innervation. However, the arms can be short and in some cases synapses are made in the absence of arms, directly on to the muscle sarcomere region (e.g. spicule protractors, MUSCLES OF THE MALE, Part II).

MaleMusTABLE1: Summary of muscle attributes

Muscle class Muscles within this class Male-specific WA abbreviation
Number
Attached to:
Electrically coupled to muscles: Innervated by:

Diagonal

(mu male diag)

diagonal yes dgl(L/R)
15 (7L, 8R)

lateral and ventral body wall, ailL/R

ailL/R

adjacent dgl

CPn (White, 1988)

R1AL,R4AL, R7AL

(right side nd)

Longitudinal

(mu male long)

anterior outer longitudinal yes aol(L/R)
2
lateral body wall
nd nd
posterior outer longitudinal yes pol(L/R)
2
lateral body wall
nd R3AL
anterior inner longitudinal yes ail(L/R)
2

ventral body wall

pilL/R

nd nd
posterior inner longitudinal yes pil(L/R)
2
ventral body wall

ailL/R

nd

nd

caudal longitudinal yes cdl(L/R)
2
lateral body wall
nd

R4BL, R4BR

Spicule

(mu male spic)

spicule protractors

yes

dorsal: dsp(L/R)

ventral: vsp(L/R)

2

 

2

dspL/R: proctodeum, spicules, adp

vspL/R: vbody wall, proctodeum, spicules

adp, vsp(L/R)

 

dspL/R

SPCR/L

 

SPCR/L

spicule retractors yes

dorsal: dsr(L/R),

 

 

 

ventral: vsr (L/R)

2

 

 

 

2

dsr(L/R): dorsal-sublateral body wall, proctodeum, spicules

 

 

 

vsr(L/R): dorsal-sublateral bodywall, spicule, proctodeum

dsr(L/R): dBWM, vsr on same side

 

 

 

vsr(L/R): dsr on same side

 

nd
mu male gub (4) gubernacular erector yes gec(L, R)
2

dorsal sublateral body wall, proctodeum, gubernaculum

nd PCAR/L, PCBL
gubernacular retractor yes grt(L, R)
2

lateral body wall, proctodeum, gubernaculum

nd PCAL
mu male obl (4) anterior oblique yes aob(L/R)
2

lateral body wall

ventral body wall

nd PCAR/L, PCBR, PCCR/L
posterior oblique yes pob(L/R)
2

lateral body wall

ventral body wall

nd PCAR/L, PCBR/L, PCCR/L
mu anal (1) anal depressor no, but modified in males adp
1

dorsal body wall, dsp(L/R), proctodeum, gubernaculum, ventral body wall

dsp(L/R) SPCL, SPCR
mu sph (1) sphincter no, but modified in males sph
1
dorsal body wall
nd nd
ventral body wall muscle no, but probably modified in males vBWM
nd nd
dorsal body wall muscle no, but modified in males dBWM

dsrL/R

DVA, DX1,DX2

nd

nd, not determined

Sources: The Male Wiring project; Sulston J.E., Albertson, D.G. and Thomson J. N., unpublished

Development of the male muscle system

Sexual specialization of the male muscle system beings in L2 and continues through to the final (L4-adult) molt. Sex-specific differences derive from two sources (1) the M-lineage, which generates 41 sex muscles not present in hermaphrodites and (2) male-specific modification of certain juvenile muscles that are common to both sexes.

1. Male-specific (M-derived) muscles

During late L2 the M lineage of the male executes a different lineage from that in the hermaphrodite and produces 3 bilateral pairs of Sex Myoblasts (SM1-3L/R) (MaleMusFIG3A, 3B). As in the hermaphrodite, SMs migrate from their birth position but move in the opposite direction, towards the tail instead of anteriorly (Sulston and Horvitz, 1977; Sulston et al., 1980; Cavallo and Stern, 2000). During L3 the SMs divide 2 or 3 times to generate 41 male-specific muscles (the sex muscles ;MaleMusFIG3A,4A-D). SM3L(left) and SM3R(right) have identical lineages, while the SM1left/right homologs as well as those of SM2 produce non-identical lineages (summarized in MaleMusFIG3B). Lineage execution is accompanied by a number of short-range migrations (see Sulston et al., 1980 Figure 27 for details).

 

2. Sexually dimorphic muscles

Some tail muscles that are present in larvae of both sexes become modified in the male late in development to function in mating behavior or copulation. These alterations can be subtle, such as the establishment of connections between non-sex-specific muscles and male-specific muscles or neurons. For example, dorsal body wall muscles, present in both sexes, can be considered sexually dimorphic because they establish gap junctions with spicule retractor muscles in the male (MUSCLES OF THE MALE, Part II, MaleMusFIG17C). Other modifications are more striking, for example, the anal depressor (adp) and the sphincter (sph) undergo extensive morphological and functional changes in the male but not in the hermaphrodite (Sulston et al., 1980).

The male anal depressor (adp): In both male and hermaphrodite larvae the adp is an H-shaped cell connecting the dorsal body wall to the roof of the rectum (MaleMusFIG5). Muscle myofilaments run dorsoventrally (D/V) and their contraction lifts the roof of the anus to allow defecation (MaleMusFIG6A). During male L4 lethargus, the adp substantially changes its shape and its contacts. The cell tilts forwards slightly but does not completely lose its contact with the dorsal roof (MaleMusFIG5). Ventrally, the anterior edges of the cell grow forward so that they meet the dorsal spicule protractor muscles and form attachments with these cells (described in MUSCLES OF THE MALE, Part II). The myofilaments within the muscle reorient so that they now run anteroposteriorly (A/P) (MaleMusFIG6B), the same direction as the spicule protractor (Sulston and Horvitz, 1977; Sulston et al., 1980). Thus the adp becomes an extension of the dorsal spicule protractors.

The male sphincter (sph): Late in male development the sphincter is functionally and morphologically altered to compensate for a newly formed connection between the alimentary and reproductive tracts (MaleMusFIG5; Sulston et al., 1980). The muscle becomes enlarged (hypertrophied) and sends an extension dorsally which attaches to the body wall roof. Intrinsic activity of the muscle and its response to GABA, which regulates defecation, are also altered (Reiner and Thomas, 1995; see MUSCLES OF THE MALE, Part II).

Diagonal muscles

The adult male has 15 diagonal muscles (dgl's) organized in a herring-bone-like fashion along either side of the ventral midline; 8 muscles on the right side (dglR), 7 on the left (dglL) (MaleMusFIG7,8A; Sulston et al., 1980).

Viewed by polarized light or with muscle myofilament markers, the dgl's appear to contain 3 sarcomeres (MaleMusFIG8B; Waterston, 1988). However, the myofilament banding patterning obseved in electron micrographs suggests possibly fewer. Along their dorsal edges, the muscles attach to the body wall at the lateral seam and along their ventral edge near the ventral midline (MaleMusFIG8C,8D,9B). The attachment points are localized at the ends of the muscle cells as half I bands ending in hemidesmosomes (Hd) and connect the myofilaments to basal lamina (Bl). The basal lamina is connected to Hds in the hyp and the hyp in turn to cuticle (red arrows, MaleMusFIG8C,9A,9B; see MESODERMAL ORGANS, Part II - Hermaphrodite Handbook for a detailed description of such structures). Diagonal muscles are also connected to other muscles, namely the inner longitudinal muscles (ailL/R, pilL/R). The muscles are joined via attachment plaques (muscle::muscle attachment complexes - yellow arrows in MaleMusFIG12D, for attachment plaque description see MESODERMAL ORGANS, Part II - Hermaphrodite Handbook).

 

During mating when males reach the end of the hermaphrodite they execute a turn to flip to the other side (MaleMusFIG10A). This turn requires ventral curling of the tail facilitated by contraction of diagonal and other tail muscles. The diagonal muscles are innervated by the male-specific CP motor neurons of the ventral cord (White, 1988). These neurons are required for precise execution of the turn (Loer and Kenyon, 1993). Serotonin (5HT) produced by the CP neurons may be responsible for stimulating diagonal muscle contraction during turning as exposure of males to exogenous serotonin can induce ventral tail curling (MaleMusFIG10B).

 

Longitudinal muscles

Three sets of longitudinal muscles are generated by the M lineage and contribute to the body wall musculature of the male (Sulston et al., 1980; MaleMusFIG11): (1) the anterior (aolL/R) and posterior (polL/R) OUTER longitudinal muscles, positioned just below the seam (MaleMusFIG12A,13A,13B); (2) the caudal OUTER longitudinal muscles (cdlL/R), which replace pol(L/R) in the tail (MaleMusFIG13B); (3) the anterior (ailL/R) and posterior (pilL/R) INNER longitudinal muscles, positioned on either side of the ventral midline (MaleMusFIG12B,13B).

In contrast to other sex muscles of the male which are non-straited, the longitudinal muscles, particularly ail(L/R), pil(L/R) and cdl(L/R), are striated, like their body wall muscle neighbors (BWM) (Sulston J.E., Albertson, D.G. and Thomson J. N., unpublished). They contain significantly more sarcomeres than non-striated muscles and attach to the body wall cuticle at multiple sites along their length (in contrast to non-striated muscles which attach only at their ends; MaleMusFIG12B,12C,12D, 14).

ails and pils are joined via attachment plaques and by gap junctions to diagonal muscles (Sulston J.E., Albertson, D.G. and Thomson J. N., unpublished). The longitudinal muscles may therefore function with diagonal muscles in turning (MaleMusFIG14A, 14B). Consistent with this possibility, the posterior outer longitudinal muscles receive inputs from the rays, which have been shown to play a role in turning (MaleMusFIG14C; Liu and Sternberg, 1995). These NMJs occur on the muscle sarcomere, and not on muscle arms, as the neuron enters the commissures to the preanal ganglion.

 

 


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