The class I myosin genes are conserved in diverse organisms, and their gene products are involved in actin dynamics, endocytosis, and signal transduction. Drosophila melanogaster has three class I myosin genes, Myosin 31DF (Myo31DF), Myosin 61F (Myo61F), and Myosin 95E (Myo95E). Myo31DF, Myo61F, and Myo95E belong to the Myosin ID, Myosin IC, and Myosin IB families, respectively. Previous loss-of-function analyses of Myo31DF and Myo61F revealed important roles in left-right (LR) asymmetric development and enterocyte maintenance, respectively. However, it was difficult to elucidate their roles in vivo, because of potential redundant activities. Here we generated class I myosin double and triple mutants to address this issue. We found that the triple mutant was viable and fertile, indicating that all three class I myosins were dispensable for survival. A loss-of-function analysis revealed further that Myo31DF and Myo61F, but not Myo95E, had redundant functions in promoting the dextral LR asymmetric development of the male genitalia. Myo61F overexpression is known to antagonize the dextral activity of Myo31DF in various Drosophila organs. Thus, the LR-reversing activity of overexpressed Myo61F may not reflect its physiological function. The endogenous activity of Myo61F in promoting dextral LR asymmetric development was observed in the male genitalia, but not the embryonic gut, another LR asymmetric organ. Thus, Myo61F and Myo31DF, but not Myo95E, play tissue-specific, redundant roles in LR asymmetric development. Our studies also revealed differential colocalization of the class I myosins with filamentous (F)-actin in the brush border of intestinal enterocytes.KEYWORDS myosin I; Myosin 31DF; Myosin 61F; Myosin 95E; left-right asymmetry T HE class I myosin genes encode myosin heavy chains, which are conserved in phylogenetically diverse organisms (Sellers 2000;Krendel and Mooseker 2005). The class I myosins are nonfilamentous, actin-based motor proteins and were the first discovered unconventional myosin proteins. These myosins are involved in a variety of cellular processes, such as cell migration, cell adhesion, and cell growth, through their regulation of actin dynamics, endocytosis, and signal transduction (Osherov and May 2000;Krendel and Mooseker 2005;Kim and Flavell 2008;McConnell and Tyska 2010).The structure of the myosin I heavy chains is evolutionarily conserved and composed of head (or motor), neck, and tail domains ( Figure 1A) (Coluccio 1997;Barylko et al. 2000). The head domain binds to filamentous (F)-actin and adenosine triphosphate (ATP), a common feature of myosin proteins ( Figure 1A) (Mermall et al. 1998); the neck domain possesses one or more IQ motifs, which directly interact with calmodulin or calmodulin-related myosin light chains (Coluccio 1997;Barylko et al. 2000), and the tail domains are divided into short and long types. Short tails contain a single tail homology 1 (TH1) domain, which is rich in basic residues and thought to interact with plasma membranes (Coluccio 1997;Barylko...

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Animal morphology and behavior often appear to evolve cooperatively. However, it is difficult to assess how strictly these two traits depend on each other. The genitalia morphologies and courtship behaviors in insects, which vary widely, may be a good model for addressing this issue. In Diptera, phylogenetic analyses of mating positions suggested that the male-above position evolved from an end-to-end one. However, with this change in mating position, the dorsoventral direction of the male genitalia became upside down with respect to that of the female genitalia. It was proposed that to compensate for this incompatibility, the male genitalia rotated an additional 180° during evolution, implying evolutionary cooperativity between the mating position and genitalia direction. According to this scenario, the proper direction of male genitalia is critical for successful mating. Here, we tested this hypothesis using a Drosophila Myosin31DF (Myo31DF) mutant, in which the rotation of the male genitalia terminates prematurely, resulting in various deviations in genitalia direction. We found that the proper dorsoventral direction of the male genitalia was a prerequisite for successful copulation, but it did not affect the other courtship behaviors. Therefore, our results suggested that the male genitalia rotation and mating position evolved cooperatively in Drosophila.

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