Sexual reproduction provides ample opportunity for pairwise interactions between the genotypes of mating pairs. One consequence of processes that are rife with male x female interactions is that evolution may fail to optimize functions for either sex, and instead there is retained a high level of variation. This appears to be the case for factors influencing sperm competition and other reproductive fitness attributes in Drosophila. The seminal proteins known as accessory gland proteins (Acps) appear to be specialized for mediating aspects of these interactions, and along with the female molecules that interact with Acps, they serve as a molecular entr? to quantifying specific male x female interactions. Our first specific aim is to use genetic isolates from natural populations to quantify male x female interactions in components of reproductive fitness with a focus on those likely to be mediated by Accessory Gland Proteins and the proteins processes with which they interact in females. Using lines from the Drosophila Genetic Reference Panel (for which both genome sequence and gene expression data are already available), supplemented where appropriate with additional lines from five broad geographic regions, we will examine male x female interactions both within and between lines and regions in a 20 x 20 partial diallel design. Paternity success in doubly-mated females, fecundity, fertility, and female remating receptivity will all be systematically scored. This study will quantify reproductive fitness components for validation of the findings of Aims 2 and 3.
The second aim i s to dissect male x female interactions by testing RNAi knockdowns of specific male Acp genes across a range of well-characterized wild female genotypes. Comparison of the same reproductive phenotypes will be scored using males that express Acps normally, or are knocked down by RNAi for specific Acps. We will begin with a focus on Acps that have been associated with effects on sperm storage and/or sperm competition. In addition, we will examine a specific test case in which both the male and female partners are known, by testing for interactions among variant alleles in Sex Peptide and the Sex Peptide receptor. Female lines that are hyper- and hyporesponsive to each knockdown will be identified, and we will partition total interaction into components mediated by each Acp. By extending our understanding of the genetic variation in male and female contributors to reproduction, we will obtain insights into how and why genetic variation is maintained in nature. Moreover, since the genes whose variation we examine involve basic reproductive functions, our results will expand the foundation for understanding cases of idiopathic human infertility, specifically those in which no sex-specific cause for the infertility can be identified and may thus reflect genetic incompatibility between the partners.

Public Health Relevance

Using Drosophila melanogaster as a model to quantify the male x female genotypic interactions in components of fertility, this project aims to understand cases of aberrant fertility of particular genotype-pairs in crosses, when neither genotype by itself is unusual in its fertility. This project has significance to understanding why large amounts of genetic diversity are maintained naturally within a species. It may also be relevant to explaining the basis for human infertilities that arise from a reproductive incompatibility between the particular pair of individuals involved.

Agency
National Institute of Health (NIH)
Institute
Eunice Kennedy Shriver National Institute of Child Health & Human Development (NICHD)
Type
Research Project (R01)
Project #
1R01HD059060-01A1
Application #
7651731
Study Section
Genetic Variation and Evolution Study Section (GVE)
Program Officer
Taymans, Susan
Project Start
2009-08-24
Project End
2011-07-31
Budget Start
2009-08-24
Budget End
2010-07-31
Support Year
1
Fiscal Year
2009
Total Cost
$381,302
Indirect Cost
Name
Cornell University
Department
Biochemistry
Type
Schools of Arts and Sciences
DUNS #
872612445
City
Ithaca
State
NY
Country
United States
Zip Code
14850
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Billeter, Jean-Christophe; Wolfner, Mariana F (2018) Chemical Cues that Guide Female Reproduction in Drosophila melanogaster. J Chem Ecol 44:750-769
Chapman, Tracey; Wolfner, Mariana F (2017) Reproductive behaviour: Make love, then war. Nat Ecol Evol 1:174
Ahmed-Braimah, Yasir H; Unckless, Robert L; Clark, Andrew G (2017) Evolutionary Dynamics of Male Reproductive Genes in the Drosophila virilis Subgroup. G3 (Bethesda) 7:3145-3155
Delbare, Sofie Y N; Chow, Clement Y; Wolfner, Mariana F et al. (2017) Roles of Female and Male Genotype in Post-Mating Responses in Drosophila melanogaster. J Hered 108:740-753
Sitnik, Jessica L; Gligorov, Dragan; Maeda, Robert K et al. (2016) The Female Post-Mating Response Requires Genes Expressed in the Secondary Cells of the Male Accessory Gland in Drosophila melanogaster. Genetics 202:1029-41
Chow, Clement Y; Kelsey, Keegan J P; Wolfner, Mariana F et al. (2016) Candidate genetic modifiers of retinitis pigmentosa identified by exploiting natural variation in Drosophila. Hum Mol Genet 25:651-9
Grenier, Jennifer K; Arguello, J Roman; Moreira, Margarida Cardoso et al. (2015) Global diversity lines - a five-continent reference panel of sequenced Drosophila melanogaster strains. G3 (Bethesda) 5:593-603
Chow, Clement Y; Avila, Frank W; Clark, Andrew G et al. (2015) Induction of excessive endoplasmic reticulum stress in the Drosophila male accessory gland results in infertility. PLoS One 10:e0119386
Chow, Clement Y; Wang, Xu; Riccardi, David et al. (2015) The genetic architecture of the genome-wide transcriptional response to ER stress in the mouse. PLoS Genet 11:e1004924

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