Seminal fluid protein

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Heliconius erato, or the red postman, was among the first species of butterfly to have its seminal fluid proteome studied. Heliconius erato 001.JPG
Heliconius erato , or the red postman, was among the first species of butterfly to have its seminal fluid proteome studied.

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.

Contents

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

Research on the function of SFPs has been conducted primarily in insect species, especially D. melanogaster. D-Melanogaster 2.jpg
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. 1 2 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. 1 2 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. 1 2 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. 1 2 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.
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