A Role for Acp29AB, a Predicted Seminal Fluid Lectin, in Female Sperm Storage in<i>Drosophila melanogaster</i>

Wong, Alex; Albright, Shannon; Giebel, Jonathan D.; Ram, K. Ravi; Ji, Shuqing; Fiumera, Anthony C.; Wolfner, Mariana F.

doi:10.1534/genetics.108.092106

Cited by 92 publications

(96 citation statements)

References 70 publications

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“…Sperm storage contains multiple steps that ensure the efficiency of the process, with these steps regulated by several seminal proteins (Acps) received by the female during mating (17)(18)(19)(20)(21). The Acps we studied here are influential in at least two ways: (1) by affecting the number of sperm that get stored (Acp36DE) and (2) by affecting the number of sperm that are retained within the SSOs (19), which could underlie their effects on males' success in sperm competition situations.…”

Section: Resultsmentioning

confidence: 99%

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Acp36DE is required for uterine conformational changes in mated Drosophila females

Avila

Wolfner

2009

Proc. Natl. Acad. Sci. U.S.A.

114

134

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In a multitude of animals with internal fertilization, including insects and mammals, sperm are stored within a female's reproductive tract after mating. Defects in the process of sperm storage drastically reduce reproductive success. In Drosophila males, ''Acp'' seminal proteins alter female postmating physiology and behavior, and are necessary for several aspects of sperm storage. For example, Acps cause a series of conformational changes in the mated female's reproductive tract that occur during and immediately after mating. These conformational changes have been hypothesized to aid both in the movement of sperm within the female and in the subsequent storage of those sperm. We used RNAi to systematically knock down several Acps involved in sperm storage to determine whether they played a role in the mating-induced uterine conformational changes. Mates of males lacking the glycoprotein Acp36DE, which is needed for the accumulation of sperm in the storage organs, fail to complete the full sequence of the conformational changes. Our results show that uterine conformational changes are important for proper accumulation of sperm in storage and identify a seminal protein that mediates these changes. Four Acps included in this study, previously shown to affect sperm release from storage (CG9997, CG1656, CG1652, and CG17575), are not necessary for uterine conformational changes to occur. Rather, consistent with their role in later steps of sperm storage, we show here that their presence can affect the outcome of sperm competition situations.reproduction ͉ seminal protein ͉ sperm competition ͉ sperm storage

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Section: Resultsmentioning

confidence: 99%

“…The process of sperm storage involves several different steps: the entry of sperm into storage, their retention and maintenance in storage, and their release from storage (1). In D. melanogaster, Acps have been shown to be necessary for sperm storage, and individual steps of the process appear to be controlled separately by different Acps (17)(18)(19)(20)(21).…”

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Acp36DE is required for uterine conformational changes in mated Drosophila females

Avila

Wolfner

2009

Proc. Natl. Acad. Sci. U.S.A.

114

134

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“…Previous work in Drosophila has demonstrated that male genotype (Clark et al 1995(Clark et al , 1999Fiumera et al 2005Fiumera et al , 2007Civetta et al 2008;Chow et al 2010), female genotype (Clark et al 1995(Clark et al , 1999Clark and Begun 1998;Civetta et al 2008;Chow et al 2010) male · female genotype interactions (Clark and Begun 1998;Clark et al 1999;Chow et al 2010) are all important to the outcome of sperm competition and that each aspect involves dozens of genes. Functional and association studies demonstrated that several male-derived accessory gland proteins (Acps) play important roles in sperm competition (Harshman and Prout 1994;Fiumera et al 2005Fiumera et al , 2007Wong et al 2008;Avila and Wolfner 2009;Chow et al 2010). However, while different female genotypes associate with differences in sperm competition outcomes, little is known about the specific genes or gene variants that underlie the differences in the female side of sperm competition.…”

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confidence: 99%

“…Functional and association studies demonstrated that several male-derived accessory gland proteins (Acps) play important roles in sperm competition (Harshman and Prout 1994;Fiumera et al 2005Fiumera et al , 2007Wong et al 2008;Avila and Wolfner 2009;Chow et al 2010). However, while different female genotypes associate with differences in sperm competition outcomes, little is known about the specific genes or gene variants that underlie the differences in the female side of sperm competition.…”

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confidence: 99%

Large Neurological Component to Genetic Differences Underlying Biased Sperm Use in Drosophila

2013

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Sperm competition arises as a result of complex interactions among male and female factors. While the roles of some male factors are known, little is known of the molecules or mechanisms that underlie the female contribution to sperm competition. The genetic tools available for Drosophila allow us to identify, in an unbiased manner, candidate female genes that are critical for mediating sperm competition outcomes. We first screened for differences in female sperm storage and use patterns by characterizing the natural variation in sperm competition in a set of 39 lines from the sequenced Drosophila Genetic Reference Panel (DGRP) of wild-derived inbred lines. We found extensive female variation in sperm competition outcomes. To generate a list of candidate female genes for functional studies, we performed a genome-wide association mapping, utilizing the common single-nucleotide polymorphisms (SNPs) segregating in the DGRP lines. Surprisingly, SNPs within ion channel genes and other genes with roles in the nervous system were among the top associated SNPs. Knockdown studies of three candidate genes (para, Rab2, and Rim) in sensory neurons innervating the female reproductive tract indicate that some of these candidate female genes may affect sperm competition by modulating the neural input of these sensory neurons to the female reproductive tract. More extensive functional studies are needed to elucidate the exact role of all these candidate female genes in sperm competition. Nevertheless, the female nervous system appears to have a previously unappreciated role in sperm competition. Our results indicate that the study of female control of sperm competition should not be limited to female reproductive tract-specific genes, but should focus also on diverse biological pathways. I N many organisms, sperm competition is an important source of reproductive variation and is critical to the reproductive success of both males and females. Sperm competition occurs when a female mates with and stores sperm from multiple males. Multiple mating creates a situation in which the males' sperm "compete" for successful fertilizations. While the ultimate outcome of a sperm competition depends on a complex interaction between male and female factors, the sexes often have different interests. Males are essentially in competition with other males, and while natural selection drives males to become better competitors with each other, it may result in males damaging the female through toxicity of seminal proteins (Wigby and Chapman 2004;Mueller et al. 2007). On the other hand, females benefit from simply being able to produce the most and highest-fitness offspring, and this may entail a specific response to male-produced molecules that influence sperm competition. The sexual conflict that arises from these different evolutionary goals of males and females implies that the genetic response to selection on sperm competition may be totally distinct in males and females. It remains largely unknown what genes drive this sexual antagon...

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“…These changes are mediated by Acp36DE, an SFP required for efficient accumulation of sperm into storage (Neubaum and Wolfner 1999;Bloch Qazi and Wolfner 2003;Avila and Wolfner 2009). Upon entry into storage, sperm are maintained in the storage organs before they are released for utilization; both of these mechanisms are influenced by SFPs (Ravi Ram and Wolfner 2007a;Wong et al 2008). Here, we determined the role of SP in sperm dynamics by examining uterine conformation, total sperm storage, sperm release, and sperm competition in the presence or absence of SP in the male ejaculate.…”

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Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females

et al. 2010

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The Drosophila seminal fluid protein (SFP) sex peptide (SP) elicits numerous post-mating responses, including increased egg laying and decreased sexual receptivity, in the mated female. Unlike other SFPs, which are detectable in mated females for only a few hours post mating, SP is maintained-and its effects are sustained-for several days. The persistence of SP in the mated female's reproductive tract is thought to be a consequence of its binding to, and gradual release from, sperm in storage, which maintains SP's ability to act within the female reproductive tract. Recent studies have shown that several other SFPs, acting in a network, are needed for SP's localization to sperm and are necessary for the efficient release of sperm from storage. This result suggested an additional new role for SP modulating the release of sperm from storage. We tested for this possibility by examining sperm storage parameters in mated females that did not receive SP. We found that while sperm accumulation into storage was unaffected, sperm depletion from storage sites was significantly decreased (or impaired) in the absence of SP. Mates of males expressing a modified SP that is unable to be released from sperm showed a similar phenotype, indicating that release of sperm-bound SP is a necessary component of normal sperm depletion. Additionally, SP null males were more successful in a sperm competitive environment when they were first to mate, which is likely a consequence of higher retention of their sperm due to defective sperm release. Our findings illustrate a direct role for SP in the release of sperm from storage.

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A Role for Acp29AB, a Predicted Seminal Fluid Lectin, in Female Sperm Storage inDrosophila melanogaster

Cited by 92 publications

References 70 publications

Acp36DE is required for uterine conformational changes in mated Drosophila females

Acp36DE is required for uterine conformational changes in mated Drosophila females

Large Neurological Component to Genetic Differences Underlying Biased Sperm Use in Drosophila

Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females

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