Diversity-Enhancing Selection Acts on a Female Reproductive Protease Family in Four Subspecies of<i>Drosophila mojavensis</i>

Kelleher, Erin S.; Clark, Nathan L.; Markow, Therese A.

doi:10.1534/genetics.110.124743

Cited by 14 publications

(13 citation statements)

References 81 publications

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“…Most of the spermatophore proteins found in P. rapae are enzymes (n = 27; 42.8%), including 11 proteases. The abundance and diversity of proteases are a recurring characteristic of ejaculates in insects and more divergent taxonomic groups (43)(44)(45). There were also many proteins of undetermined function.…”

Section: Envelope and Inner Matrix Are Composed Of Distinct Protein Smentioning

confidence: 99%

Structural complexity and molecular heterogeneity of a butterfly ejaculate reflect a complex history of selection

Meslin

Cherwin

Plakke

et al. 2017

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

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Male ejaculates are often structurally complex, and this complexity is likely to influence key reproductive interactions between males and females. However, despite its potential evolutionary significance, the molecular underpinnings of ejaculate structural complexity have received little empirical attention. To address this knowledge gap, we sought to understand the biochemical and functional properties of the structurally complex ejaculates of butterflies. Males in this species produce large ejaculates called spermatophores composed of an outer envelope, an inner matrix, and a bolus of sperm. Females are thought to benefit from the nutrition contained in the soluble inner matrix through increases in longevity and fecundity. However, the indigestible outer envelope of the spermatophore delays female remating, allowing males to monopolize paternity for longer. Here, we show that these two nonsperm-containing spermatophore regions, the inner matrix and the outer envelope, differ in their protein composition and functional properties. We also reveal how these divergent protein mixtures are separately stored in the male reproductive tract and sequentially transferred to the female reproductive tract during spermatophore assembly. Intriguingly, we discovered large quantities of female-derived proteases in both spermatophore regions shortly after mating, which may contribute to spermatophore digestion and hence, female control over remating rate. Finally, we report evidence of past selection on these spermatophore proteins and female proteases, indicating a complex evolutionary history. Our findings illustrate how structural complexity of ejaculates may allow functionally and/or spatially associated suites of proteins to respond rapidly to divergent selective pressures, such as sexual conflict or reproductive cooperation.

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Section: Envelope and Inner Matrix Are Composed Of Distinct Protein Smentioning

confidence: 99%

Structural complexity and molecular heterogeneity of a butterfly ejaculate reflect a complex history of selection

Meslin

Cherwin

Plakke

et al. 2017

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

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“…The identification of bursa proteases and proteases inhibitors is in agreement with results from a distant Lepidopteran, the European Corn Borer moth ( Al-Wathiqui et al 2014 ). Furthermore, proteolytic cascades are well known to be involved in reproductive interactions between males and females over a wide range of taxonomic groups ( Kelleher et al 2007 , 2011 ). Because the spermatophore is a complex structure composed of lipids, proteins, and carbohydrates, we explored two additional functional categories potentially important in spermatophore digestion: carbohydrate processing and lipid processing.…”

Section: Resultsmentioning

confidence: 99%

Digestive Organ in the Female Reproductive Tract Borrows Genes from Multiple Organ Systems to Adopt Critical Functions

Meslin

Plakke

Deutsch

et al. 2015

Molecular Biology and Evolution

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Persistent adaptive challenges are often met with the evolution of novel physiological traits. Although there are specific examples of single genes providing new physiological functions, studies on the origin of complex organ functions are lacking. One such derived set of complex functions is found in the Lepidopteran bursa copulatrix, an organ within the female reproductive tract that digests nutrients from the male ejaculate or spermatophore. Here, we characterized bursa physiology and the evolutionary mechanisms by which it was equipped with digestive and absorptive functionality. By studying the transcriptome of the bursa and eight other tissues, we revealed a suite of highly expressed and secreted gene products providing the bursa with a combination of stomach-like traits for mechanical and enzymatic digestion of the male spermatophore. By subsequently placing these bursa genes in an evolutionary framework, we found that the vast majority of their novel digestive functions were co-opted by borrowing genes that continue to be expressed in nonreproductive tissues. However, a number of bursa-specific genes have also arisen, some of which represent unique gene families restricted to Lepidoptera and may provide novel bursa-specific functions. This pattern of promiscuous gene borrowing and relatively infrequent evolution of tissue-specific duplicates stands in contrast to studies of the evolution of novelty via single gene co-option. Our results suggest that the evolution of complex organ-level phenotypes may often be enabled (and subsequently constrained) by changes in tissue specificity that allow expression of existing genes in novel contexts, such as reproduction. The extent to which the selective pressures encountered in these novel roles require resolution via duplication and sub/neofunctionalization is likely to be determined by the need for specialized reproductive functionality. Thus, complex physiological phenotypes such as that found in the bursa offer important opportunities for understanding the relative role of pleiotropy and specialization in adaptive evolution.

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“…It is now clear that a large fraction of sex-biased genes may result from gene duplication of preexisting sex-biased genes [82, 84, 85, 152, 153]. This has occurred multiple times in some gene families (e.g., female reproductive proteases or accessory gland proteins [83–85]).…”

Section: The Contribution Of Gene Duplication To Sex-biased Expresmentioning

confidence: 99%

Gene Duplication and the Genome Distribution of Sex-Biased Genes

Gallach

Domingues

Betrán

2011

International Journal of Evolutionary Biology

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In species that have two sexes, a single genome encodes two morphs, as each sex can be thought of as a distinct morph. This means that the same set of genes are differentially expressed in the different sexes. Many questions emanate from this statement. What proportion of genes contributes to sexual dimorphism? How do they contribute to sexual dimorphism? How is sex-biased expression achieved? Which sex and what tissues contribute the most to sex-biased expression? Do sex-biased genes have the same evolutionary patterns as nonbiased genes? We review the current data on sex-biased expression in species with heteromorphic sex chromosomes and comment on the most important hypotheses suggested to explain the origin, evolution, and distribution patterns of sex-biased genes. In this perspective we emphasize how gene duplication serves as an important molecular mechanism to resolve genomic clashes and genetic conflicts by generating sex-biased genes, often sex-specific genes, and contributes greatly to the underlying genetic basis of sexual dimorphism.

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Diversity-Enhancing Selection Acts on a Female Reproductive Protease Family in Four Subspecies ofDrosophila mojavensis

Cited by 14 publications

References 81 publications

Structural complexity and molecular heterogeneity of a butterfly ejaculate reflect a complex history of selection

Structural complexity and molecular heterogeneity of a butterfly ejaculate reflect a complex history of selection

Digestive Organ in the Female Reproductive Tract Borrows Genes from Multiple Organ Systems to Adopt Critical Functions

Gene Duplication and the Genome Distribution of Sex-Biased Genes

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