Seminal fluid protein

A photo of Heliconius erato, a species of butterfly
Heliconius erato, or the red postman, was among the first species of butterfly to have its seminal fluid proteome studied.[1]

Seminal fluid proteins (SFPs) or accessory gland proteins (Acps) are one of the non-sperm components of semen. In many animals with internal fertilization, males transfer a complex cocktail of proteins in their semen to females during copulation. These seminal fluid proteins often have diverse, potent effects on female post-mating phenotypes.[2] SFPs are produced by the male accessory glands.

Seminal fluid proteins frequently show evidence of elevated evolutionary rates and are often cited as an example of sexual conflict.[2]

Proteomics

SFPs are best studied in mammals and insects,[3] especially in the common fruit fly, Drosophila melanogaster. Most species produce a wide variety of proteins that are transferred to females. For example, approximately 290 SFPs have been identified in D. melanogaster,[4][5][6] 46 in the mosquito Anopheles gambae,[7] and around 160 in humans.[8]

Elevated evolution

Even between closely related species, the seminal fluid proteome can vary greatly. SFPs show elevated rates of DNA sequence change compared to non-reproductive genes (measured by Ka/Ks ratio) in many orders, including Diptera (flies),[9][10] Lepidoptera (butterflies and moths),[1] Rodentia,[11] and Primates.[12][13][14]

Additionally, SFPs show high rates of gene turnover compared to non-reproductive genes.[10]

Function

Mating drosophila melanogaster.
Research on the function of SFPs has been conducted primarily in insect species, especially D. melanogaster.

The function of SFPs is best understood in D. melanogaster. SFPs play a role in male–male sperm competition. One study that manipulated the amount of SFPs male D. melanogaster produced found that when males were in competition, males that produced more SFPs sired a larger proportion of offspring.[15] Many D. melanogaster SFP genes are expressed by the female reproductive tract, particularly within the sperm storage organs, which may be more consistent with roles supporting spermatozoa than in sexual conflict. [16]

In many insect species, significant changes occur in female behavior and physiology following mating; the isolated receipt of SFPs has been shown to be responsible for many of these changes. In D. melanogaster females, over 160 genes show either up or down-regulation following isolated SFP receipt.[17] These transcriptomic changes are not limited to the female's reproductive tract.[18] SFPs lengthen the refractory period (when the female is disinterested in mating) and stimulate ovulation; additionally they can affect processes such as sperm storage, metabolism, and activity levels.[3]

Though SFPs seem to play a role in coordinating male and female reproductive efforts (e.g. in timing of ovulation), SFPs may also be a source of sexual conflict. Studies of D. melanogaster have revealed that females who received SFPs suffered decreased lifespan and fitness.[19] Frequent mating in D. melanogaster is associated with a reduction in female lifespan,[20] and this cost of mating in females has been shown to be primarily mediated by receipt of SFPs.[21]

As SFPs play an important role in reproductive processes in disease-carrying species of mosquito and additionally tend to be highly species-specific, manipulation of SFPs may hold potential for highly targeted control of these mosquito populations.[22]

References

  1. ^ a b Walters, J. R.; Harrison, R. G. (2010-04-07). "Combined EST and Proteomic Analysis Identifies Rapidly Evolving Seminal Fluid Proteins in Heliconius Butterflies". Molecular Biology and Evolution. 27 (9): 2000–2013. doi:10.1093/molbev/msq092. ISSN 0737-4038. PMID 20375075.
  2. ^ a b Sirot, Laura K.; Wong, Alex; Chapman, Tracey; Wolfner, Mariana F. (2014-12-11). "Sexual Conflict and Seminal Fluid Proteins: A Dynamic Landscape of Sexual Interactions". Cold Spring Harbor Perspectives in Biology. 7 (2): a017533. doi:10.1101/cshperspect.a017533. ISSN 1943-0264. PMC 4315932. PMID 25502515.
  3. ^ a b Avila, Frank W.; Sirot, Laura K.; LaFlamme, Brooke A.; Rubinstein, C. Dustin; Wolfner, Mariana F. (2011). "Insect Seminal Fluid Proteins: Identification and Function". Annual Review of Entomology. 56: 21–40. doi:10.1146/annurev-ento-120709-144823. ISSN 0066-4170. PMC 3925971. PMID 20868282.
  4. ^ Findlay, Geoffrey D.; Yi, Xianhua; MacCoss, Michael J.; Swanson, Willie J. (2008-07-29). "Proteomics Reveals Novel Drosophila Seminal Fluid Proteins Transferred at Mating". PLOS Biology. 6 (7): e178. doi:10.1371/journal.pbio.0060178. ISSN 1545-7885. PMC 2486302. PMID 18666829.
  5. ^ Findlay, Geoffrey D.; MacCoss, Michael J.; Swanson, Willie J. (2009-05-01). "Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila". Genome Research. 19 (5): 886–896. doi:10.1101/gr.089391.108. ISSN 1088-9051. PMC 2675977. PMID 19411605.
  6. ^ Wigby, Stuart; Brown, Nora C.; Allen, Sarah E.; Misra, Snigdha; Sitnik, Jessica L.; Sepil, Irem; Clark, Andrew G.; Wolfner, Mariana F. (2020-12-07). "The Drosophila seminal proteome and its role in postcopulatory sexual selection". Philosophical Transactions of the Royal Society B: Biological Sciences. 375 (1813): 20200072. doi:10.1098/rstb.2020.0072. ISSN 0962-8436. PMC 7661438. PMID 33070726.
  7. ^ Dottorini, Tania; Nicolaides, Lietta; Ranson, Hilary; Rogers, David W.; Crisanti, Andrea; Catteruccia, Flaminia (2007-10-09). "A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior". Proceedings of the National Academy of Sciences. 104 (41): 16215–16220. Bibcode:2007PNAS..10416215D. doi:10.1073/pnas.0703904104. ISSN 0027-8424. PMC 2042187. PMID 17901209.
  8. ^ Schumacher, Julia; Rosenkranz, David; Herlyn, Holger (2014-01-22). "Mating systems and protein–protein interactions determine evolutionary rates of primate sperm proteins". Proceedings of the Royal Society of London B: Biological Sciences. 281 (1775): 20132607. doi:10.1098/rspb.2013.2607. ISSN 0962-8452. PMC 3866406. PMID 24307672.
  9. ^ Kelleher, Erin S; Watts, Thomas D; Laflamme, Brooke A; Haynes, Paul A; Markow, Therese A (2009-05-01). "Proteomic analysis of Drosophila mojavensis male accessory glands suggests novel classes of seminal fluid proteins". Insect Biochemistry and Molecular Biology. 39 (5–6): 366–371. Bibcode:2009IBMB...39..366K. doi:10.1016/j.ibmb.2009.03.003. ISSN 0965-1748. PMID 19328853.
  10. ^ a b Mueller, J. L. (2005-06-18). "Cross-Species Comparison of Drosophila Male Accessory Gland Protein Genes". Genetics. 171 (1): 131–143. doi:10.1534/genetics.105.043844. ISSN 0016-6731. PMC 1456506. PMID 15944345.
  11. ^ Ramm, S. A.; McDonald, L.; Hurst, J. L.; Beynon, R. J.; Stockley, P. (2008-10-06). "Comparative Proteomics Reveals Evidence for Evolutionary Diversification of Rodent Seminal Fluid and Its Functional Significance in Sperm Competition". Molecular Biology and Evolution. 26 (1): 189–198. doi:10.1093/molbev/msn237. ISSN 0737-4038. PMID 18931385.
  12. ^ Clark, Nathaniel L.; Swanson, Willie J. (2005). "Pervasive Adaptive Evolution in Primate Seminal Proteins". PLOS Genetics. 1 (3): e35. doi:10.1371/journal.pgen.0010035. ISSN 1553-7390. PMC 1201370. PMID 16170411.
  13. ^ Good, Jeffrey M.; Wiebe, Victor; Albert, Frank W.; Burbano, Hernán A.; Kircher, Martin; Green, Richard E.; Halbwax, Michel; André, Claudine; Atencia, Rebeca (2013-01-16). "Comparative Population Genomics of the Ejaculate in Humans and the Great Apes". Molecular Biology and Evolution. 30 (4): 964–976. doi:10.1093/molbev/mst005. ISSN 1537-1719. PMID 23329688.
  14. ^ Meslin, Camille; Laurin, Michel; Callebaut, Isabelle; Druart, Xavier; Monget, Philippe (2015). "Evolution of species-specific major seminal fluid proteins in placental mammals by gene death and positive selection". Contributions to Zoology. 84 (3): 217–235. doi:10.1163/18759866-08403003.
  15. ^ Wigby, Stuart; Sirot, Laura K.; Linklater, Jon R.; Buehner, Norene; Calboli, Federico C.F.; Bretman, Amanda; Wolfner, Mariana F.; Chapman, Tracey (May 2009). "Seminal Fluid Protein Allocation and Male Reproductive Success". Current Biology. 19 (9): 751–757. Bibcode:2009CBio...19..751W. doi:10.1016/j.cub.2009.03.036. ISSN 0960-9822. PMC 2737339. PMID 19361995.
  16. ^ Thayer, Rachel C.; Polston, Elizabeth S.; Xu, Jixiang; Begun, David J. (2024-10-29). "Regional specialization, polyploidy, and seminal fluid transcripts in the Drosophila female reproductive tract". Proceedings of the National Academy of Sciences. 121 (44): e2409850121. doi:10.1073/pnas.2409850121. ISSN 0027-8424. PMC 11536144. PMID 39453739.
  17. ^ McGraw, Lisa A.; Gibson, Greg; Clark, Andrew G.; Wolfner, Mariana F. (August 2004). "Genes Regulated by Mating, Sperm, or Seminal Proteins in Mated Female Drosophila melanogaster". Current Biology. 14 (16): 1509–1514. Bibcode:2004CBio...14.1509M. doi:10.1016/j.cub.2004.08.028. ISSN 0960-9822. PMID 15324670. S2CID 17056259.
  18. ^ McGraw, L. A.; Clark, A. G.; Wolfner, M. F. (2008-06-18). "Post-mating Gene Expression Profiles of Female Drosophila melanogaster in Response to Time and to Four Male Accessory Gland Proteins". Genetics. 179 (3): 1395–1408. doi:10.1534/genetics.108.086934. ISSN 0016-6731. PMC 2475742. PMID 18562649.
  19. ^ Wigby, Stuart; Chapman, Tracey (February 2005). "Sex Peptide Causes Mating Costs in Female Drosophila melanogaster". Current Biology. 15 (4): 316–321. Bibcode:2005CBio...15..316W. doi:10.1016/j.cub.2005.01.051. ISSN 0960-9822. PMID 15723791. S2CID 15533396.
  20. ^ Fowler, Kevin; Partridge, Linda (April 1989). "A cost of mating in female fruitflies". Nature. 338 (6218): 760–761. Bibcode:1989Natur.338..760F. doi:10.1038/338760a0. ISSN 0028-0836. S2CID 4283317.
  21. ^ Chapman, Tracey; Liddle, Lindsay F.; Kalb, John M.; Wolfner, Mariana F.; Partridge, Linda (January 1995). "Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products". Nature. 373 (6511): 241–244. Bibcode:1995Natur.373..241C. doi:10.1038/373241a0. ISSN 0028-0836. PMID 7816137. S2CID 4336339.
  22. ^ "Grant explores using seminal fluid proteins to control mosquitoes | Cornell Chronicle". news.cornell.edu. Retrieved 2018-08-14.