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Evolutionary Expressed Sequence Tag Analysis of Drosophila Female Reproductive Tracts Identifies Genes Subjected to Positive Selection

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Evolutionary Expressed Sequence Tag Analysis of Drosophila Female Reproductive Tracts Identifies Genes Subjected to Positive Selection Copyright 2004 by the Genetics Society of America DOI: 10.1534/genetics.104.030478 Evolutionary Expressed Sequence Tag Analysis of Drosophila Female Reproductive Tracts Identifies Genes Subjected to Positive Selection Willie J. Swanson,*,†,1 Alex Wong,† Mariana F. Wolfner† and Charles F. Aquadro† *Department of Genome Sciences, University of Washington, Seattle, Washington 98195-7730 and †Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853-2703 Manuscript received April 23, 2004 Accepted for publication August 10, 2004 ABSTRACT Genes whose products are involved in reproduction include some of the fastest-evolving genes found within the genomes of several organisms. Drosophila has long been used to study the function and evolutionary dynamics of genes thought to be involved in sperm competition and sexual conflict, two processes that have been hypothesized to drive the adaptive evolution of reproductive molecules. Several seminal fluid proteins (Acps) made in the Drosophila male reproductive tract show evidence of rapid adaptive evolution. To identify candidate genes in the female reproductive tract that may be involved in female–male interac- tions and that may thus have been subjected to adaptive evolution, we used an evolutionary bioinformatics approach to analyze sequences from a cDNA library that we have generated from Drosophila female reproduc- tive tracts. We further demonstrate that several of these genes have been subjected to positive selection. Their expression in female reproductive tracts, presence of signal sequences/transmembrane domains, and rapid adaptive evolution indicate that they are prime candidates to encode female reproductive molecules that interact with rapidly evolving male Acps. ENES whose products participate in reproduction genome demonstrated that the genes encoding Acps G often show signs of adaptive evolution (Swanson are on average twice as divergent as non-Acp genes and Vacquier 2002). For example, two-dimensional gel (Swanson et al. 2001a). Although no statistically signifi- electrophoresis has shown that proteins from Drosoph- cant departures from neutrality were observed in the ila male and female reproductive organs are, on average, tests applied in their study, 11% of the ESTs identified twice as diverse between species as those from nonrepro- by Swanson et al. (2001a) showed a signature consistent ductive tissues (Civetta and Singh 1995). A similar with adaptive evolution by virtue of having a d N/d S ratio pattern has been found at the nucleotide level for Dro- greater than one. sophila male accessory gland proteins (Acps)(Aguade´ Although the nature and evolution of several repro- et al. 1992; Tsaur and Wu 1997; Aguade´ 1998, 1999; ductive molecules contributed by the male have been Tsaur et al. 1998; Begun et al. 2000; Swanson et al. studied in detail, relatively little is known about the 2001a; Kern et al. 2004). Acps are important compo- evolution of female reproductive molecules. The few nents of the seminal fluid of the male ejaculate and cases studied so far suggest that adaptive evolution may have been shown to have a variety of effects on the also occur in female reproductive molecules. Positive mated female (Wolfner 2002). Acps have been shown selection on female reproductive molecules has been to increase the female’s egg laying rate (Herndon and detected in mammals (Swanson et al. 2001b, 2003; Wolfner 1995; Soller et al. 1997, 1999; Heifetz et al. Jansa et al. 2003) and abalone (Galindo et al. 2003). 2000, 2001; Chapman et al. 2003; Liu and Kubli 2003), Here we present the first systematic attempt to identify reduce her receptivity to remating (Chen et al. 1988; genes encoding female reproductive proteins in Dro- Chapman et al. 2003; Liu and Kubli 2003), decrease sophila and to initiate evolutionary analyses of several the female’s lifespan (Chapman et al. 1995), and be such genes. involved in sperm storage and utilization (Neubaum To this end, we have undertaken an evolutionary EST and Wolfner 1999; Tram and Wolfner 1999; Xue and screen of the reproductive tract of female Drosophila. Noll 2000). An analysis of expressed sequence tags Proteins produced in the female reproductive tract carry (ESTs) derived from Drosophila simulans male accessory out a variety of important physiological functions. Pro- glands and compared to the completed D. melanogaster cesses such as sperm storage, control of oogenesis and ovulation, and control over remating rate are likely to involve interactions between female molecules and mol- ecules transferred from the male to the female. For 1Corresponding author: Department of Genome Sciences, University of Washington, Seattle, WA 98195-7730. example, the male seminal fluid proteins Acp36DE and E-mail: [email protected] Acp62F localize to the sperm storage organs following Genetics 168: 1457–1465 (November 2004) 1458 W. J. Swanson et al. mating (Neubaum and Wolfner 1999; Lung et al. 2002), San Diego). We did not perform in-solution subtractive hybrid- Acp26Aa localizes to the base of the ovary (Heifetz et ization or normalize the cDNA library because these methods typically result in truncated cDNAs, and we desired full-length al. 2000), and sex peptide (Acp70A) binds to receptors cDNA for our evolutionary comparisons. The resulting library in the female genital tract (Ottiger et al. 2000). Thus, contained 130,000 CFUs, of which 99% were recombinant. we expect that some proteins expressed in the female The average insert size was 1.2 kb. Two sets of probes were reproductive tract will interact molecularly with Acps, utilized for differential hybridization. First, oligo(dT)-primed sperm, or other components of the male ejaculate. Mol- first-strand male cDNA was prepared from mixed age and mating status whole adult male D. simulans flies using Bethesda ecules secreted into the female reproductive tract may Research Laboratories (Gaithersburg, MD) superscript II re- also carry out a variety of functions, such as egg activa- verse transcriptase incorporating 32P-labeled dCTP and then tion, lubrication, or defense against pathogens, that do denatured at 65Њ for 30 min in 0.3 m NaOH. Second, a random- not necessitate any molecular contribution from the primed probe was generated from a mixture of RT-PCR prod- male (Wolfner et al. 2004). ucts from the three female yolk protein genes from D. melano- gaster: YP1, YP2, and YP3 (Barnett et al. 1980). These genes Our first goal in carrying out this EST screen was to were screened out of the library since yolk protein RNAs are identify a suite of genes whose products can be consid- abundantly expressed in the fat body, which is associated with ered candidate female reproductive molecules. Since a the reproductive tract (Barnett et al. 1980) (they are also recurring observation about reproductive proteins is expressed in the ovary, which was removed). Hybridization Њ ϫ ϫ that many show adaptive divergence (Swanson and was for 18 hr at 65 in 5 SSPE, 5 Denhardt’s, 0.5% SDS, 0.2 mg/ml salmon sperm DNA. Final washes were at 65Њ, 0.1ϫ Vacquier 2002), we also incorporate evolutionary infor- SSPE for 10 min. Sequencing was from QIAGEN purified mation into our screen by deriving ESTs from D. sim- plasmid DNA using ABI big dye terminator sequencing chem- ulans (a close relative of D. melanogaster) and aligning istry analyzed on an ABI 3100 automated sequencer. EST them to their putative orthologs in the completed D. sequences are deposited in GenBank under accession nos. melanogaster genome (Adams et al. 2000). We identified CO391819–CO392724, CO408479, and CO408480. Polymorphism survey: DNA was extracted using the Pure- 526 genes that show enriched expression in the female Gene DNA isolation kit from isofemale lines of D. melanogaster reproductive tract, 169 of which encode predicted extra- and D. simulans previously collected by C. Aquadro in Belts- cellular or cell surface molecules that could interact ville, Maryland. To maximize the power of our statistical tests, with male proteins during reproduction. we focused our analyses on intron regions, which should max- Our second goal, given the interspecific amino acid imize variation within and between species under neutrality. PCR primers and conditions are available as online supple- sequence diversity that has been observed for Drosoph- mentary material at http://www.genetics.org/supplemental/. ila male accessory gland genes (Tsaur and Wu 1997; PCR products were diluted eightfold with water and se- Aguade´ 1998, 1999; Tsaur et al. 1998; Begun et al. 2000; quenced directly using ABI big dye terminator sequencing Swanson et al. 2001a; Kern et al. 2004), was to determine chemistry and analyzed on an ABI 3100 automated sequencer. if there is a similar level of diversity among female Dro- Sequences are deposited in GenBank under accession nos. sophila reproductive molecules. Analysis of nucleotide AY665365–AY665396. Divergence study: We assessed DNA sequence divergence sequence polymorphism within and/or divergence among among five to eight increasingly divergent species of Drosoph- Drosophila species reveal statistically robust evidence that ila for five genes. For each we used either all or overlapping at least six genes expressed in the female reproductive subsets of the following species: D. erecta, D. eugracilis, D. lutescens, tract show signs consistent with having been subjected D. melanogaster, D. pseudoobscura, D. simulans, D. teissieri, and D. to positive selection and identify 25 additional candidates yakuba (detailed in
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