Gene duplication and adaptive evolution of digestive proteases in Drosophila arizonae female reproductive tracts - PubMed (original) (raw)

Gene duplication and adaptive evolution of digestive proteases in Drosophila arizonae female reproductive tracts

Erin S Kelleher et al. PLoS Genet. 2007 Aug.

Abstract

It frequently has been postulated that intersexual coevolution between the male ejaculate and the female reproductive tract is a driving force in the rapid evolution of reproductive proteins. The dearth of research on female tracts, however, presents a major obstacle to empirical tests of this hypothesis. Here, we employ a comparative EST approach to identify 241 candidate female reproductive proteins in Drosophila arizonae, a repleta group species in which physiological ejaculate-female coevolution has been documented. Thirty-one of these proteins exhibit elevated amino acid substitution rates, making them candidates for molecular coevolution with the male ejaculate. Strikingly, we also discovered 12 unique digestive proteases whose expression is specific to the D. arizonae lower female reproductive tract. These enzymes belong to classes most commonly found in the gastrointestinal tracts of a diverse array of organisms. We show that these proteases are associated with recent, lineage-specific gene duplications in the Drosophila repleta species group, and exhibit strong signatures of positive selection. Observation of adaptive evolution in several female reproductive tract proteins indicates they are active players in the evolution of reproductive tract interactions. Additionally, pervasive gene duplication, adaptive evolution, and rapid acquisition of a novel digestive function by the female reproductive tract points to a novel coevolutionary mechanism of ejaculate-female interaction.

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Conflict of interest statement

Competing interests. The authors have declared that no competing interests exist.

Figures

Figure 1

Figure 1. Functional Composition of Candidate Female Reproductive Proteins

Functional composition of 241 secreted and transmembrane proteins in D. arizonae female reproductive tracts based on GO terms [59].

Figure 2

Figure 2. Distribution of Three Protease Gene Families in D. mojavensis and D. virilis Genomes

(A) Syntenic regions of protease gene family 1: D. mojavensis Chromosome 4 (scaffold_6680, bp 10216565–10169309) and D. virilis Chromosome 3 (scaffold_13049, bp 10558802–10608251). (B) protease gene family 2: D. mojavensis Chromosome 3 (scaffold_6500, bp 18241557– 18296199) and D. virilis Chromosome 4 (scaffold_12963, bp 15263878–15319561). (C) protease gene family 3: D. mojavensis Chromosome 3 (scaffold_6500, bp 20970182–21063420) and D. virilis chromosome 4 (scaffold_12963 bp 12250368–12347919). Colored blocks indicate individual exons, where each gene is indicated by a different color. Orthologous genes are the same color in both species, and connected by colored lines. Solid lines indicate orthologs with the same orientation, while dotted lines indicate inverted orthologs. Multiple, tandemly duplicated copies in the genome of D. mojavensis correspond to a single gene in the genome of D. virilis. Annotation and assembly obtained from unpublished Drosophila genomes (

http://rana.lbl.gov/drosophila/

).

Figure 3

Figure 3. Bayesian Phylogenies of (A) Protease Gene Family 1, (B) Protease Gene Family 2, and (C) Protease Gene Family 3

(A) is midpoint rooted, as D. virilis sequence was too divergent to make an appropriate outgroup. Grey taxon name denotes a pseudogene. Branch colors indicate Ka/Ks values calculated in the codeml package of PAML [47]. Posterior probabilities < 90 are noted.

Figure 4

Figure 4. RT-PCR of Three Gene Families

Universal primers for each gene family were used to amplify genomic DNA, and cDNA from males, female carcasses (no lower reproductive tract), and lower reproductive tracts (for complete gels see Figure S1).

Figure 5

Figure 5. Structural Models Generated in SWISS-MODEL

(A) protease gene family 1and (B) protease gene family 2. The blue amino acids comprise the catalytic triad of the active site. The aquamarine amino acids are determinants of substrate specificity [48]. The red amino acids indicate positively selected sites. The labeled amino acid in (A), 216, is a positively selected amino acid that is also a determinant of substrate specificity.

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