Seminal fluid protein

Last updated
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]

Related Research Articles

<i>Drosophila</i> Genus of flies

Drosophila is a genus of fly, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or pomace flies, vinegar flies, or wine flies, a reference to the characteristic of many species to linger around overripe or rotting fruit. They should not be confused with the Tephritidae, a related family, which are also called fruit flies ; tephritids feed primarily on unripe or ripe fruit, with many species being regarded as destructive agricultural pests, especially the Mediterranean fruit fly.

<i>Drosophila melanogaster</i> Species of fruit fly

Drosophila melanogaster is a species of fly in the family Drosophilidae. The species is often referred to as the fruit fly or lesser fruit fly, or less commonly the "vinegar fly", "pomace fly", or "banana fly". In the wild, D. melanogaster are attracted to rotting fruit and fermenting beverages, and are often found in orchards, kitchens and pubs.

<span class="mw-page-title-main">Epididymis</span> Tube that connects a testicle to a vas deferens

The epididymis is an elongated tubular genital organ attached to the posterior side of each one of the two male reproductive glands, the testicles. It is a single, narrow, tightly coiled tube in adult humans, 6 to 7 centimetres in length; uncoiled the tube would be approximately 6 m long. It connects the testicle to the vas deferens in the male reproductive system. The epididymis serves as an interconnection between the multiple efferent ducts at the rear of a testicle (proximally), and the vas deferens (distally). Its primary function is the storage, maturation and transport of sperm cells.

<span class="mw-page-title-main">Sperm competition</span> Reproductive process

Sperm competition is the competitive process between spermatozoa of two or more different males to fertilize the same egg during sexual reproduction. Competition can occur when females have multiple potential mating partners. Greater choice and variety of mates increases a female's chance to produce more viable offspring. However, multiple mates for a female means each individual male has decreased chances of producing offspring. Sperm competition is an evolutionary pressure on males, and has led to the development of adaptations to increase male's chance of reproductive success. Sperm competition results in a sexual conflict between males and females. Males have evolved several defensive tactics including: mate-guarding, mating plugs, and releasing toxic seminal substances to reduce female re-mating tendencies to cope with sperm competition. Offensive tactics of sperm competition involve direct interference by one male on the reproductive success of another male, for instance by mate guarding or by physically removing another male's sperm prior to mating with a female. For an example, see Gryllus bimaculatus.

The mechanisms of reproductive isolation are a collection of evolutionary mechanisms, behaviors and physiological processes critical for speciation. They prevent members of different species from producing offspring, or ensure that any offspring are sterile. These barriers maintain the integrity of a species by reducing gene flow between related species.

<span class="mw-page-title-main">Sexual conflict</span> Term in evolutionary biology

Sexual conflict or sexual antagonism occurs when the two sexes have conflicting optimal fitness strategies concerning reproduction, particularly over the mode and frequency of mating, potentially leading to an evolutionary arms race between males and females. In one example, males may benefit from multiple matings, while multiple matings may harm or endanger females due to the anatomical differences of that species. Sexual conflict underlies the evolutionary distinction between male and female.

<i>Drosophila pseudoobscura</i> Species of fly

Drosophila pseudoobscura is a species of fruit fly, used extensively in lab studies of speciation. It is native to western North America.

<span class="mw-page-title-main">Mating plug</span> Gelatinous secretion used in the mating of some species

A mating plug, also known as a copulation plug, sperm plug, vaginal plug, or sphragis, is a gelatinous secretion used in the mating of some species. It is deposited by a male into a female genital tract, such as the vagina, and later hardens into a plug or glues the tract together. While females can expel the plugs afterwards, the male's sperm still gets a time advantage in getting to the egg, which is often the deciding factor in fertilization.

Cytoplasmic incompatibility (CI) is a mating incompatibility reported in many arthropod species that is caused by intracellular parasites such as Wolbachia. These bacteria reside in the cytoplasm of the host cells and modify their hosts' sperm in a way that leads to embryo death unless this modification is 'rescued' by the same bacteria in the eggs. CI has been reported in many insect species, as well as in mites and woodlice. Aside from Wolbachia, CI can be induced by the bacteria Cardinium,Rickettsiella, Candidatus Mesenet longicola and Spiroplasma. CI is currently being exploited as a mechanism for Wolbachia-mediated disease control in mosquitoes.

Bateman's principle, in evolutionary biology, is that in most species, variability in reproductive success is greater in males than in females. It was first proposed by Angus John Bateman (1919–1996), an English geneticist. Bateman suggested that, since males are capable of producing millions of sperm cells with little effort, while females invest much higher levels of energy in order to nurture a relatively small number of eggs, the female plays a significantly larger role in their offspring's reproductive success. Bateman's paradigm thus views females as the limiting factor of parental investment, over which males will compete in order to copulate successfully.

<span class="mw-page-title-main">Female sperm storage</span>

Female sperm storage is a biological process and often a type of sexual selection in which sperm cells transferred to a female during mating are temporarily retained within a specific part of the reproductive tract before the oocyte, or egg, is fertilized. This process takes place in some species of animals. The site of storage is variable among different animal taxa and ranges from structures that appear to function solely for sperm retention, such as insect spermatheca and bird sperm storage tubules, to more general regions of the reproductive tract enriched with receptors to which sperm associate before fertilization, such as the caudal portion of the cow oviduct containing sperm-associating annexins. Female sperm storage is an integral stage in the reproductive process for many animals with internal fertilization. It has several documented biological functions including:

<span class="mw-page-title-main">Male accessory gland</span> Sexual gland in males

Male accessory glands (MAG) are the seminal vesicles, prostate gland, and the bulbourethral glands. These glands are found only in mammals. In insects, male accessory glands produce products that mix with the sperm to protect and preserve them, including seminal fluid proteins. Some insecticides can induce an increase in the protein content of the male accessory glands of certain types of insects. This has the unintended effect of increasing the number of offspring they produce.

Sexual antagonistic co-evolution is the relationship between males and females where sexual morphology changes over time to counteract the opposite's sex traits to achieve the maximum reproductive success. This has been compared to an arms race between sexes. In many cases, male mating behavior is detrimental to the female's fitness. For example, when insects reproduce by means of traumatic insemination, it is very disadvantageous to the female's health. During mating, males will try to inseminate as many females as possible, however, the more times a female's abdomen is punctured, the less likely she is to survive. Females that possess traits to avoid multiple matings will be more likely to survive, resulting in a change in morphology. In males, genitalia is relatively simple and more likely to vary among generations compared to female genitalia. This results in a new trait that females have to avoid in order to survive.

Interlocus sexual conflict is a type of sexual conflict that occurs through the interaction of a set of antagonistic alleles at two or more different loci, or the location of a gene on a chromosome, in males and females, resulting in the deviation of either or both sexes from the fitness optima for the traits. A co-evolutionary arms race is established between the sexes in which either sex evolves a set of antagonistic adaptations that is detrimental to the fitness of the other sex. The potential for reproductive success in one organism is strengthened while the fitness of the opposite sex is weakened. Interlocus sexual conflict can arise due to aspects of male–female interactions such as mating frequency, fertilization, relative parental effort, female remating behavior, and female reproductive rate.

<i>Drosophila hydei</i> Species of fly

Drosophila hydei (mosca casera) is a species of Diptera, or the order of flies, in the family Drosophilidae. It is a species in the hydei species subgroup, a group in the repleta species group. Bizarrely, it is also known for having approximately 23 mm long sperm, 10 times the length of the male's body. Drosophila hydei are commonly found on compost piles worldwide, and can be rudimentarily identified by eye owing to their large size and variegated pigment pattern on the thorax. The name derives from Dr R. R. Hyde, who first discovered that the species was distinct from Drosophila repleta. D. hydei are one of the more popular flies used as feeders in the pet trade. A few varieties are available, some flightless. They are very similar to Drosophila melanogaster, despite having separated 50 million years ago.

Most insects reproduce oviparously, i.e. by laying eggs. The eggs are produced by the female in a pair of ovaries. Sperm, produced by the male in one testicle or more commonly two, is transmitted to the female during mating by means of external genitalia. The sperm is stored within the female in one or more spermathecae. At the time of fertilization, the eggs travel along oviducts to be fertilized by the sperm and are then expelled from the body ("laid"), in most cases via an ovipositor.

Spiroplasma poulsonii are bacteria of the genus Spiroplasma that are commonly endosymbionts of flies. These bacteria live in the hemolymph of the flies, where they can act as reproductive manipulators or defensive symbionts.

<i>Drosophila quinaria</i> species group Species group of the subgenus Drosophila

The Drosophila quinaria species group is a speciose lineage of mushroom-feeding flies studied for their specialist ecology, their parasites, population genetics, and the evolution of immune systems. Quinaria species are part of the Drosophila subgenus.

Mariana Federica Wolfner is the Goldwin Smith Professor of molecular biology and genetics at Cornell University. Her research investigates sexual conflict in the fruit fly Drosophila melanogaster. She was elected a member of the National Academy of Sciences (NAS) in 2019 in recognition of her distinguished and continuing achievements in original research.

Drosophila metlerri, commonly known as the Sonoran Desert fly, is a fly in the genus Drosophila. The species is found in North America and is most concentrated along the southern coast of California and in Mexico. D. mettleri are dependent on plant hosts, namely, the saguaro and cardon cacti. Thus, they are most prevalent in arid, desert conditions. It is able to detoxify chemicals found in the rotting liquid of cacti hosts, which allows it to use otherwise lethal soil as a nesting site.

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.