The muscle of Lawrence in Drosophila : A case of repeated evolutionary loss

Abstract

The muscle of Lawrence (MOL) is a bilaterally symmetrical muscle spanning the tergite of the fifth abdominal segment of adult male Drosophila melanogaster. It is not, however, a general feature of male-specific development within the subfamily Drosophilinae. Of 95 species surveyed within this subfamily, 67 exist with no MOL at all. By drawing comparisons with published cladograms of species relatedness, three conclusions regarding the evolutionary history of the MOL are made: (i) The MOL predates the major radiations of the genus Drosophila, given its presence in earlierbranching Chymomyza and Scaptodrosophila; the MOL has been subsequently excluded in at least one present species of each of these two primitive genera. First described in Drosophila melanogaster, the muscle of Lawrence (MOL) is a large, bilaterally symmetrical muscle spanning the fifth tergite of the abdomen of adult males; it does not develop in females (1). Oddly, the MOL eluded decades of extensive genetic and biological investigation in D. melanogaster, including the definitive survey of adult musculature by Miller in 1950 (2). Only in 1984 was this muscle's existence first revealed with the report of Lawrence (the muscle's eponym) and Johnston (1), showing that formation of the MOL is sex-specific and is associated with developmental cues in the fifth abdominal segment (A5) of the male; homeotic mutations transforming either A4 or A6 to A5 induce the development of a MOL in the transformed segment (1, 3).Development of the MOL depends not on the sex of its progenitor myoblasts, but rather the sex of the contacting motoneuron in A5. If the motoneuron is male, the MOL develops; if the motoneuron is female, the MOL fails to develop (3). Ablation of the ingrowing motoneuron in a male correspondingly blocks MOL development (4). Although use of the MOL to the adult male fly is unknown, other interesting observations have accumulated regarding its general biology, including genetic evidence that its development requires normal expression of fruitless (fru) (5, 6), a gene identified by its involvement in adult male courtship behavior (7) and as a sex determination gene that acts late in development (8, 9). In addition, formation of the MOL in A5 involves recruitment of the relatively rare 79B actin (10).To gain insight into the evolutionary history of this muscle, we have analyzed its appearance within the subfamily Drosophilinae. Surprisingly, of 95 species surveyed, 67 have no MOL at all. By comparing our observations with generally accepted cladograms of species relatedness within the Drosophilinae (11-24), we provide evidence that the MOL was an existing feature of primitive forms within the early radiation of the subfamily. Also stemming from that comparison is our conclusion that several independent genetic exclusions of this muscle have occurred during the subsequent radiation of MOL-containing lines. This makes the MOL a rare example of an anatomical structure that has undergone independent, repeated loss among closely related evolut...

Variation in fiber number of a male‐specific muscle between Drosophila species: a genetic and developmental analysis

“…In agreement with our observations, it can be noted that in Fig. 1 of Gailey et al (1997), D. sechellia and D. mauritiana MOL appear larger than D. melanogaster and D. simulans MOL.…”

“…The muscle of Lawrence (MOL), a male-specific abdominal muscle, is present in many drosophilid species and has apparently been lost multiple times during Drosophila evolution (Gailey et al 1997). For example, the MOL is absent in half of the species of the Drosophila melanogaster species subgroup (Gailey et al 1997 and this article).…”

Evolution of male sexual characters in the Oriental Drosophila melanogaster species group

“…1 and 2C). Secondary loss has also been reported for another sexually dimorphic trait in Drosophila , a male‐specific abdominal muscle (the so‐called Muscle of Lawrence; Lawrence and Johnston 1984; Gailey et al 1997. Recent phylogenetic studies demonstrate that loss of male sexual traits is common in a variety of animals; one possible explanation is that female mating preferences (and therefore sexual selection) may often disappear or reverse direction (Wiens 2001).…”

SPECIES-SPECIFIC PATTERNS OF SEXUAL DIMORPHISM IN THE EXPRESSION OF FRUITLESS PROTEIN, A NEURAL MUSCULINIZING FACTOR INDROSOPHILA

“…The total number of mFru expressing cells is largest in D. yakuba ($ 240); it is smallest in D. ananassae ($130) (Table I). It should be emphasized that the males of D. ananassae, D. virilis and D. yakuba do not have the MOL (Gailey et al, 1997), yet they express mFru in the ventral ganglia in which the somata of motoneurons innervating abdominal muscles are expected to be located (Fig. 2).…”

“…Interestingly, there are species whose males lack the MOL or have an additional set of MOLs in A4 (Gailey et al, 1997). However, it has not been explored whether species differences in mFru expression in neurons correlate with the observed variations in the MOL among the species.…”