The Soup in My Fly: Evolution, Form and Function of Seminal Fluid Proteins

Tracey Chapman

doi:10.1371/journal.pbio.0060179

Sperm wars and the evolution of male fertility

Reproduction ◽

10.1530/rep-12-0285 ◽

2012 ◽

Vol 144 (5) ◽

pp. 519-534 ◽

Cited By ~ 210

Author(s):

Leigh W Simmons ◽

John L Fitzpatrick

Keyword(s):

Sperm Competition ◽

Swimming Speed ◽

Male Fertility ◽

Seminal Fluid ◽

Future Research ◽

Sperm Length ◽

Seminal Fluid Proteins ◽

Control Male ◽

Form And Function ◽

And Function

Females frequently mate with several males, whose sperm then compete to fertilize available ova. Sperm competition represents a potent selective force that is expected to shape male expenditure on the ejaculate. Here, we review empirical data that illustrate the evolutionary consequences of sperm competition. Sperm competition favors the evolution of increased testes size and sperm production. In some species, males appear capable of adjusting the number of sperm ejaculated, depending on the perceived levels of sperm competition. Selection is also expected to act on sperm form and function, although the evidence for this remains equivocal. Comparative studies suggest that sperm length and swimming speed may increase in response to selection from sperm competition. However, the mechanisms driving this pattern remain unclear. Evidence that sperm length influences sperm swimming speed is mixed and fertilization trials performed across a broad range of species demonstrate inconsistent relationships between sperm form and function. This ambiguity may in part reflect the important role that seminal fluid proteins (sfps) play in affecting sperm function. There is good evidence that sfps are subject to selection from sperm competition, and recent work is pointing to an ability of males to adjust their seminal fluid chemistry in response to sperm competition from rival males. We argue that future research must consider sperm and seminal fluid components of the ejaculate as a functional unity. Research at the genomic level will identify the genes that ultimately control male fertility.

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Molecular Diversification of the Seminal Fluid Proteome in a Recently Diverged Passerine Species Pair

Molecular Biology and Evolution ◽

10.1093/molbev/msz235 ◽

2019 ◽

Vol 37 (2) ◽

pp. 488-506 ◽

Cited By ~ 11

Author(s):

Melissah Rowe ◽

Emma Whittington ◽

Kirill Borziak ◽

Mark Ravinet ◽

Fabrice Eroukhmanoff ◽

...

Keyword(s):

Seminal Fluid ◽

Passer Domesticus ◽

Species Pair ◽

Seminal Fluid Proteins ◽

Passerine Species ◽

Immunity Genes ◽

Evolutionary Genomic ◽

Whole Genome Resequencing ◽

And Function ◽

Reproductive Processes

Abstract Seminal fluid proteins (SFPs) mediate an array of postmating reproductive processes that influence fertilization and fertility. As such, it is widely held that SFPs may contribute to postmating, prezygotic reproductive barriers between closely related taxa. We investigated seminal fluid (SF) diversification in a recently diverged passerine species pair (Passer domesticus and Passer hispaniolensis) using a combination of proteomic and comparative evolutionary genomic approaches. First, we characterized and compared the SF proteome of the two species, revealing consistencies with known aspects of SFP biology and function in other taxa, including the presence and diversification of proteins involved in immunity and sperm maturation. Second, using whole-genome resequencing data, we assessed patterns of genomic differentiation between house and Spanish sparrows. These analyses detected divergent selection on immunity-related SF genes and positive selective sweeps in regions containing a number of SF genes that also exhibited protein abundance diversification between species. Finally, we analyzed the molecular evolution of SFPs across 11 passerine species and found a significantly higher rate of positive selection in SFPs compared with the rest of the genome, as well as significant enrichments for functional pathways related to immunity in the set of positively selected SF genes. Our results suggest that selection on immunity pathways is an important determinant of passerine SF composition and evolution. Assessing the role of immunity genes in speciation in other recently diverged taxa should be prioritized given the potential role for immunity-related proteins in reproductive incompatibilities in Passer sparrows.

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BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1914491116 ◽

2019 ◽

Vol 116 (49) ◽

pp. 24719-24728 ◽

Cited By ~ 2

Author(s):

Ben R. Hopkins ◽

Irem Sepil ◽

Sarah Bonham ◽

Thomas Miller ◽

Philip D. Charles ◽

...

Keyword(s):

Seminal Fluid ◽

Cell Types ◽

Bmp Signaling ◽

Secretory Cells ◽

Normal Female ◽

Seminal Fluid Proteins ◽

Accessory Glands ◽

Offspring Production ◽

Morphogenetic Protein ◽

And Function

Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of ∼1,000 fertility-enhancing “main cells” and ∼40 more functionally cryptic “secondary cells.” Inhibition of bone morphogenetic protein (BMP) signaling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female postmating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary-cell secretions might therefore make highly specific contributions to the seminal proteome and ejaculate function; alternatively, they might regulate more global—but hitherto undiscovered—SFP functions and proteome composition. Here, we present data that support the latter model. We show that in addition to previously reported phenotypes, secondary-cell-specific BMP signaling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal changes to the seminal proteome that surprisingly encompass alterations to main-cell–derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell types, suggesting that modification to the cellular make-up of seminal-fluid-producing tissues is an important factor in ejaculate evolution.

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BMP-signalling inhibition in Drosophila secondary cells remodels the seminal proteome, and self and rival ejaculate functions

10.1101/741587 ◽

2019 ◽

Author(s):

Ben R. Hopkins ◽

Irem Sepil ◽

Sarah Bonham ◽

Thomas Miller ◽

Philip D. Charles ◽

...

Keyword(s):

Seminal Fluid ◽

Cell Types ◽

Secretory Cells ◽

Normal Female ◽

Seminal Fluid Proteins ◽

Accessory Glands ◽

Offspring Production ◽

Use Efficiency ◽

Bmp Signalling ◽

And Function

ABSTRACTSeminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of ∼1000 fertility-enhancing ‘main cells’ and ∼40, more functionally cryptic, ‘secondary cells’. Inhibition of BMP-signalling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female post-mating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary cell secretions might therefore make a highly specific contribution to the seminal proteome and ejaculate function; alternatively, they might regulate more global – but hitherto-undiscovered – SFP functions and proteome composition. Here, we present data that supports the latter model. We show that in addition to previously reported phenotypes, secondary cell-specific BMP-signalling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a novel constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal a mix of specific and widespread changes to the seminal proteome that surprisingly encompass alterations to main cell-derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell-types suggesting that modification to the cellular make-up of seminal fluid-producing tissues is an important factor in ejaculate evolution.

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Insect Seminal Fluid Proteins: Identification and Function

Annual Review of Entomology ◽

10.1146/annurev-ento-120709-144823 ◽

2011 ◽

Vol 56 (1) ◽

pp. 21-40 ◽

Cited By ~ 493

Author(s):

Frank W. Avila ◽

Laura K. Sirot ◽

Brooke A. LaFlamme ◽

C. Dustin Rubinstein ◽

Mariana F. Wolfner

Keyword(s):

Seminal Fluid ◽

Seminal Fluid Proteins ◽

And Function

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Scanning tunneling microscopy (STM) of DNA and RNA

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100152148 ◽

1989 ◽

Vol 47 ◽

pp. 34-35

Author(s):

Patricia G. Arscott ◽

Gil Lee ◽

Victor A. Bloomfield ◽

D. Fennell Evans

Keyword(s):

Molecular Structures ◽

Inorganic Materials ◽

Resolving Power ◽

Scanning Tunneling ◽

Tunneling Microscopy ◽

Form And Function ◽

Dna And Rna ◽

Calf Thymus ◽

And Function ◽

The Relationship

STM is one of the most promising techniques available for visualizing the fine details of biomolecular structure. It has been used to map the surface topography of inorganic materials in atomic dimensions, and thus has the resolving power not only to determine the conformation of small molecules but to distinguish site-specific features within a molecule. That level of detail is of critical importance in understanding the relationship between form and function in biological systems. The size, shape, and accessibility of molecular structures can be determined much more accurately by STM than by electron microscopy since no staining, shadowing or labeling with heavy metals is required, and there is no exposure to damaging radiation by electrons. Crystallography and most other physical techniques do not give information about individual molecules.We have obtained striking images of DNA and RNA, using calf thymus DNA and two synthetic polynucleotides, poly(dG-me5dC)·poly(dG-me5dC) and poly(rA)·poly(rU).

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