Academic journal article Genetics

Cross-Species Comparison of Drosophila Male Accessory Gland Protein Genes

Academic journal article Genetics

Cross-Species Comparison of Drosophila Male Accessory Gland Protein Genes

Article excerpt

ABSTRACT

Drosophila melanogaster males transfer seminal fluid proteins along with sperm during mating. Among these proteins, ACPs (Accessory gland proteins) from the male's accessory gland induce behavioral, physiological, and life span reduction in mated females and mediate sperm storage and utilization. A previous evolutionary EST screen in D. simulans identified partial cDNAs for 57 new candidate ACPs. Here we report the annotation and confirmation of the corresponding Acp genes in D. melanogaster. Of 57 new candidate Acp genes previously reported in D. melanogaster, 34 conform to our more stringent criteria for encoding putative male accessory gland extracellular proteins, thus bringing the total number of ACPs identified to 52 (34 plus 18 previously identified). This comprehensive set of Acp genes allows us to dissect the patterns of evolutionary change in a suite of proteins from a single male-specific reproductive tissue. We used sequence-based analysis to examine codon bias, gene duplications, and levels of divergence (via d^sub N^/d^sub S^ values and ortholog detection) of the 52 D. melanogaster ACPs in D. simulans, D. yakuba, and D. pseudoobscura. We show that 58% of the 52 D. melanogaster Acp genes are detectable in D. pseudoobscura. Sequence comparisons of ACPs shared and not shared between D. melanogaster and D. pseudoobscura show that there are separate classes undergoing distinctly dissimilar evolutionary dynamics.

ACCESSORY gland proteins (ACPs) induce a variety of physiological, behavioral, and reproductive changes when transferred to the female. Between 25 and 150 ACPs were initially thought to be transferred to the female during mating (!NGMAN-BAKER and CANDIDO 1980; SCHMIDT et al 1985; WHALEN and WILSON 1986; COULTHART and SINGH 1988; WOLFNER et al. 1997). Males lacking ACPs have impaired fertility, indicating that ACPs perform important reproductive functions (KALB et al. 1993; XUE and NOLL 2000). Specifically, ACPs cause females to increase their egg-production, egg-laying, and ovulation rates, decrease their propensity to remate, and store and utilize sperm (reviewed in WOLFNER 2002; CHAPMAN and DAVIES 2004). ACPs also participate in formation of the mating plug (LuNG and WOLFNER 2001) and mediate a decrease in the mated female's life span (CHAPMAN et al. 1995). Genetic analyses have revealed the functions of four ACPs thus far. Acp26Aa (ovulin) is a prohormone that triggers an increase in ovulation rate (HERNDON and WOLFNER 1995; HEIFETZ et al. 2000). Acp36DE is a glycoprotein that is essential for sperm storage (NEUBAUM and WOLFNER 1999), by regulating sperm accumulation into storage (BLOCK QAZI and WOLFNER 2003). Acp70A (sex peptide) induces egg laying and decreases females' receptivity to remating; it also contributes to the cost of mating to females (CHEN et al. 1988; AIGAKI et al. 1991; CHAPMAN et al. 2003; LIU and KUBLI 2003; WIGBY and CHAPMAN 2005). Acp62F is a trypsin protease inhibitor that localizes to the sperm storage organs of mated females and has been suggested to preserve sperm viability (LuNG et al. 2002). Acp62F also enters the female's circulation and is toxic to flies upon repeated ectopic expression, suggesting a possible role in the life span cost of mating (LuNG et al. 2002). In addition, the transfer of antimicrobial ACPs to the female (LuNG et al. 2001) and the Acpinduced upregulation of antimicrobial peptides in mated females (LAWNICZAK and BEGUN 2004; McGRAw et al. 2004) suggests that ACPs may contribute to a female's immune defense. Altogether, ACPs appear to participate in a complex set of interactions by competing/cooperating with seminal fluid proteins of other males (CLARK et al. 1995; CLARK et al. 1999; PROUT and CLARK 1996; SNOOK and HOSKEN 2004), receptors present in the female or on sperm, and pathogens. To better understand this diverse set of interactions of ACPs it is important to fully characterize the ACPs involved and examine their evolutionary dynamics. …

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