Proteomic analysis reveals dynamic changes in cloacal fluid composition during the reproductive season in a sexually promiscuous passerine

. 2024 Jun 20 ; 14 (1) : 14259. [epub] 20240620

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38902251

Grantová podpora
1308120 Grantová Agentura, Univerzita Karlova
1308120 Grantová Agentura, Univerzita Karlova
1308120 Grantová Agentura, Univerzita Karlova
19-22538S Grantová Agentura České Republiky
19-22538S Grantová Agentura České Republiky
19-22538S Grantová Agentura České Republiky
19-22538S Grantová Agentura České Republiky
19-22538S Grantová Agentura České Republiky

Odkazy

PubMed 38902251
PubMed Central PMC11190206
DOI 10.1038/s41598-024-62244-3
PII: 10.1038/s41598-024-62244-3
Knihovny.cz E-zdroje

Cryptic female choice (CFC) is a component of postcopulatory sexual selection that allows females to influence the fertilization success of sperm from different males. While its precise mechanisms remain unclear, they may involve the influence of the protein composition of the female reproductive fluids on sperm functionality. This study maps the protein composition of the cloacal fluid across different phases of female reproductive cycle in a sexually promiscuous passerine, the barn swallow. Similar to mammals, the protein composition in the female reproductive tract differed between receptive (when females copulate) and nonreceptive phases. With the change in the protein background, the enriched gene ontology terms also shifted. Within the receptive phase, distinctions were observed between proteomes sampled just before and during egg laying. However, three proteins exhibited increased abundance during the entire receptive phase compared to nonreceptive phases. These proteins are candidates in cryptic female choice, as all of them can influence the functionality of sperm or sperm-egg interaction. Our study demonstrates dynamic changes in the cloacal environment throughout the avian breeding cycle, emphasizing the importance of considering these fluctuations in studies of cryptic female choice.

Zobrazit více v PubMed

Parker GA. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 1970;45:525–567. doi: 10.1111/j.1469-185X.1970.tb01176.x. DOI

Thornhill R. Cryptic female choice and its implications in the Scorpionfly Harpobittacus nigriceps. Am. Nat. 1983;122:765–788. doi: 10.1086/284170. DOI

Firman RC, Gasparini C, Manier MK, Pizzari T. Postmating female control: 20 years of cryptic female choice. Trends Ecol. Evol. 2017;32:368–382. doi: 10.1016/j.tree.2017.02.010. PubMed DOI PMC

Gasparini C, Pilastro A, Evans JP. The role of female reproductive fluid in sperm competition. Philos. Trans. R. Soc. B Biol. Sci. 2020;375:20200077. doi: 10.1098/rstb.2020.0077. PubMed DOI PMC

Dean R, Nakagawa S, Pizzari T. The risk and intensity of sperm ejection in female birds. Am. Nat. 2011;178:343–354. doi: 10.1086/661244. PubMed DOI

Lüpold S, et al. Female mediation of competitive fertilization success in Drosophila melanogaster. Proc. Natl. Acad. Sci. 2013;110:10693–10698. doi: 10.1073/pnas.1300954110. PubMed DOI PMC

Fitzpatrick JL, Lüpold S. Sexual selection and the evolution of sperm quality. Mol. Hum. Reprod. 2014;20:1180–1189. doi: 10.1093/molehr/gau067. PubMed DOI

Birkhead TR, Møller AP. Sexual selection and the temporal separation of reproductive events: Sperm storage data from reptiles, birds and mammals. Biol. J. Lin. Soc. 1993;50:295–311. doi: 10.1111/j.1095-8312.1993.tb00933.x. DOI

Holt WV, Lloyd RE. Sperm storage in the vertebrate female reproductive tract: How does it work so well? Theriogenology. 2010;73:713–722. doi: 10.1016/j.theriogenology.2009.07.002. PubMed DOI

Bakst M, Wishart G, Brillard J-P. Oviducal sperm selection, transport, and storage in poultry. Poult. Sci. Rev. 1994;5:117–143.

Gasparini C, Pilastro A. Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy. Proc. R. Soc. B Biol. Sci. 2011;278:2495–2501. doi: 10.1098/rspb.2010.2369. PubMed DOI PMC

Pitnick, S., Wolfner, M. F. & Suarez, S. S. Ejaculate-female and sperm-female interactions. In Sperm Biology: An Evolutionary Perspective 247–304 (Academic Press, London, 2009). 10.1016/B978-0-12-372568-4.00007-0.

Urbach D, Folstad I, Rudolfsen G. Effects of ovarian fluid on sperm velocity in Arctic charr (Salvelinus alpinus) Behav. Ecol. Sociobiol. 2005;57:438–444. doi: 10.1007/s00265-004-0876-4. DOI

Villanueva-Diaz C, Vadillo-Ortega F, Kably-Ambe A, Diaz-Pérez MA, Krivitzky SK. Evidence that human follicular fluid contains a chemoattractant for spermatozoa. Fertil. Steril. 1990;54:1180–1182. doi: 10.1016/S0015-0282(16)54027-8. PubMed DOI

Oliveira RG, Tomasi L, Rovasio RA, Giojalas LC. Increased velocity and induction of chemotactic response in mouse spermatozoa by follicular and oviductal fluids. Reproduction. 1999;115:23–27. doi: 10.1530/jrf.0.1150023. PubMed DOI

Cramer ERA, et al. Testing a post-copulatory pre-zygotic reproductive barrier in a passerine species pair. Behav. Ecol. Sociobiol. 2014;68:1133–1144. doi: 10.1007/s00265-014-1724-9. DOI

Cramer ERA, et al. Sperm performance in conspecific and heterospecific female fluid. Ecol. Evol. 2016;6:1363–1377. doi: 10.1002/ece3.1977. PubMed DOI PMC

Cramer ERA, Ålund M, McFarlane SE, Johnsen A, Qvarnström A. Females discriminate against heterospecific sperm in a natural hybrid zone. Evolution. 2016;70:1844–1855. doi: 10.1111/evo.12986. PubMed DOI

Poignet M, et al. Sperm morphology and performance in relation to postmating prezygotic isolation in two recently diverged passerine species. Sci. Rep. 2022;12:22275. doi: 10.1038/s41598-022-26101-5. PubMed DOI PMC

Ahammad MU, et al. Effects of fluid secreted from the uterus on duration of fertile egg production in hens, and survivability and penetrability of fowl sperm in vitro. J. Poult. Sci. 2013;50:74–82. doi: 10.2141/jpsa.0120045. DOI

Yeates SE, et al. Cryptic choice of conspecific sperm controlled by the impact of ovarian fluid on sperm swimming behavior. Evolution. 2013;67:3523–3536. doi: 10.1111/evo.12208. PubMed DOI PMC

Gasparini C, Evans JP. Ovarian fluid mediates the temporal decline in sperm viability in a fish with sperm storage. PLoS ONE. 2013;8:e64431. doi: 10.1371/journal.pone.0064431. PubMed DOI PMC

Turner E, Montgomerie R. Ovarian fluid enhances sperm movement in Arctic charr. J. Fish Biol. 2002;60:1570–1579. doi: 10.1111/j.1095-8649.2002.tb02449.x. DOI

Gomendio M, Roldan ERS. Implications of diversity in sperm size and function for sperm competition and fertility. Int. J. Dev. Biol. 2008;52:439–447. doi: 10.1387/ijdb.082595mg. PubMed DOI

Knief U, et al. A sex-chromosome inversion causes strong overdominance for sperm traits that affect siring success. Nat. Ecol. Evol. 2017;1:1177–1184. doi: 10.1038/s41559-017-0236-1. PubMed DOI

Lahnsteiner F, Weismann T, Patzner R. Composition of the ovarian fluid in 4 salmonid species: Oncorhynchus mykiss, Salmo trutta f lacustris, Saivelinus alpinus and Hucho hucho. Reprod. Nutr. Dev. 1995;35:465–474. doi: 10.1051/rnd:19950501. PubMed DOI

Rosengrave P, et al. Chemical composition of seminal and ovarian fluids of chinook salmon (Oncorhynchus tshawytscha) and their effects on sperm motility traits. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2009;152:123–129. doi: 10.1016/j.cbpa.2008.09.009. PubMed DOI

Ramm SA. Seminal fluid and accessory male investment in sperm competition. Philos. Trans. R. Soc. B Biol. Sci. 2020;375:20200068. doi: 10.1098/rstb.2020.0068. PubMed DOI PMC

Zadmajid V, Myers JN, Sørensen SR, Ernest Butts IA. Ovarian fluid and its impacts on spermatozoa performance in fish: A review. Theriogenology. 2019;132:144–152. doi: 10.1016/j.theriogenology.2019.03.021. PubMed DOI

Kholodnyy V, Gadêlha H, Cosson J, Boryshpolets S. How do freshwater fish sperm find the egg? The physicochemical factors guiding the gamete encounters of externally fertilizing freshwater fish. Rev. Aquac. 2019;12:1165–1192. doi: 10.1111/raq.12378. DOI

Swanson W, Vacquier V. Reproductive protein evolution. Annu. Rev. Ecol. Evol. Syst. 2002;33:161–179. doi: 10.1146/annurev.ecolsys.33.010802.150439. DOI

Lahnsteiner F. Morphological, physiological and biochemical parameters characterizing the over-ripening of rainbow trout eggs. Fish Physiol. Biochem. 2000;23:107–118. doi: 10.1023/A:1007839023540. DOI

Johnson SL, et al. Ovarian fluid proteome variation associates with sperm swimming speed in an externally fertilizing fish. J. Evol. Biol. 2020;33:1783–1794. doi: 10.1111/jeb.13717. PubMed DOI PMC

Zhang H, et al. Use of proteomic analysis of endometriosis to identify different protein expression in patients with endometriosis versus normal controls. Fertil. Steril. 2006;86:274–282. doi: 10.1016/j.fertnstert.2006.01.028. PubMed DOI

Ma X, et al. Proteomic analysis of human ovaries from normal and polycystic ovarian syndrome. Mol. Hum. Reprod. 2007;13:527–535. doi: 10.1093/molehr/gam036. PubMed DOI

Apichela SA, et al. Biochemical composition and protein profile of alpaca (Vicugna pacos) oviductal fluid. Anim. Reprod. Sci. 2015;154:79–85. doi: 10.1016/j.anireprosci.2014.12.013. PubMed DOI

Hatzirodos N, et al. Transcript abundance of stromal and thecal cell related genes during bovine ovarian development. PLoS ONE. 2019;14:e0213575. doi: 10.1371/journal.pone.0213575. PubMed DOI PMC

Nakamura O, et al. Transport of maternal transthyretin to the fetus in the viviparous teleost Neoditrema ransonnetii (Perciformes, Embiotocidae) J. Comp. Physiol. B. 2020;190:231–241. doi: 10.1007/s00360-020-01261-w. PubMed DOI

Meng Y, et al. Effects of GnRH antagonist on endometrial protein profiles in the window of implantation. Proteomics. 2014;14:2350–2359. doi: 10.1002/pmic.201400145. PubMed DOI

Muthukumar S, et al. Buffalo cervico-vaginal fluid proteomics with special reference to estrous cycle: Heat shock protein (Hsp)-70 appears to be an Estrus indicator1. Biol. Reprod. 2014;90(97):1–8. PubMed

Černá M, Kuntová B, Talacko P, Stopková R, Stopka P. Differential regulation of vaginal lipocalins (OBP, MUP) during the estrous cycle of the house mouse. Scientific Reports. 2017;7:11674. doi: 10.1038/s41598-017-12021-2. PubMed DOI PMC

Soleilhavoup C, et al. Proteomes of the female genital tract during the oestrous cycle. Mol. Cell. Proteomics. 2016;15:93–108. doi: 10.1074/mcp.M115.052332. PubMed DOI PMC

Griffith SC, Owens IPF, Thuman KA. Extra pair paternity in birds: A review of interspecific variation and adaptive function. Mol. Ecol. 2002;11:2195–2212. doi: 10.1046/j.1365-294X.2002.01613.x. PubMed DOI

Brouwer L, Griffith SC. Extra-pair paternity in birds. Mol. Ecol. 2019;28:4864–4882. doi: 10.1111/mec.15259. PubMed DOI PMC

Birkhead TR, Brillard J-P. Reproductive isolation in birds: postcopulatory prezygotic barriers. Trends Ecol. Evol. 2007;22:266–272. doi: 10.1016/j.tree.2007.02.004. PubMed DOI

Froman D. Deduction of a model for sperm storage in the oviduct of the domestic fowl (Gallus domesticus) Biol. Reprod. 2003;69:248–253. doi: 10.1095/biolreprod.102.013482. PubMed DOI

Bakst MR, Akuffo V. Alkaline phosphatase reactivity in the vagina and uterovaginal junction sperm-storage tubules of turkeys in egg production: Implications for sperm storage. Br. Poult. Sci. 2007;48:515–518. doi: 10.1080/00071660701381761. PubMed DOI

Gautron J, et al. Ovotransferrin is a matrix protein of the hen eggshell membranes and basal calcified layer. Connect. Tissue Res. 2001;42:255–267. doi: 10.3109/03008200109016840. PubMed DOI

Riou C, et al. Avian uterine fluid proteome: Exosomes and biological processes potentially involved in sperm survival. Mol. Reprod. Dev. 2020;87:454–470. doi: 10.1002/mrd.23333. PubMed DOI

Riou C, et al. Proteomic analysis of uterine fluid of fertile and subfertile hens before and after insemination. Reproduction. 2019;158:335–356. doi: 10.1530/REP-19-0079. PubMed DOI

Møller AP, Brohede J, Cuervo JJ, de Lope F, Primmer C. Extrapair paternity in relation to sexual ornamentation, arrival date, and condition in a migratory bird. Behav. Ecol. 2003;14:707–712. doi: 10.1093/beheco/arg051. DOI

Michálková R, Tomášek O, Adámková M, Kreisinger J, Albrecht T. Extra-pair paternity patterns in European barn swallows Hirundo rustica are best explained by male and female age rather than male ornamentation. Behav. Ecol. Sociobiol. 2019;73:119. doi: 10.1007/s00265-019-2725-5. DOI

Møller AP, Mousseau TA, Rudolfsen G. Females affect sperm swimming performance: A field experiment with barn swallows Hirundo rustica. Behav. Ecol. 2008;19:1343–1350. doi: 10.1093/beheco/arn068. DOI

Møller AP, et al. Senescent sperm performance in old male birds. J. Evol. Biol. 2009;22:334–344. doi: 10.1111/j.1420-9101.2008.01650.x. PubMed DOI

Møller AP. Mixed reproductive strategy and mate guarding in a semi-colonial passerine, the swallow Hirundo rustica. Behav. Ecol. Sociobiol. 1985;17:401–408. doi: 10.1007/BF00293220. DOI

Kempenaers B. Does reproductive synchrony limit male opportunities or enhance female choice for extra-pair paternity? Behavior. 1997;134:441–562. doi: 10.1163/156853997X00520. DOI

Mota PG, Hoi-Leitner M. Intense extrapair behaviour in a semicolonial passerine does not result in extrapair fertilizations. Anim. Behav. 2003;66:1019–1026. doi: 10.1006/anbe.2002.2285. DOI

Redfern CPF, Clark JA. Ringers’ Manual. British Trust for Ornithology; 2001.

Redfern CPF. Brood patches. Ringers’ Bull. 2008;12:39–41.

Petrželková A, et al. Brood parasitism and quasi-parasitism in the European barn swallow Hirundo rustica rustica. Behav. Ecol. Sociobiol. 2015;69:1405–1414. doi: 10.1007/s00265-015-1953-6. DOI

Kuntová B, Stopková R, Stopka P. Transcriptomic and proteomic profiling revealed high proportions of odorant binding and antimicrobial defense proteins in olfactory tissues of the house mouse. Front. Genet. 2018;9:297892. doi: 10.3389/fgene.2018.00026. PubMed DOI PMC

Otčenášková T, et al. Comparative sperm proteomics in selected passerine birds reflects sperm morphology and mitochondrial metabolism. J. Vertebr. Biol. 2023;72:23045.1–23114. doi: 10.25225/jvb.23045. DOI

Cox J, et al. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics. 2014;13:2513–2526. doi: 10.1074/mcp.M113.031591. PubMed DOI PMC

Crawley MJ. The R Book. Wiley; 2007.

Chawade A, Alexandersson E, Levander F. Normalyzer: A tool for rapid evaluation of normalization methods for omics data sets. J. Proteome Res. 2014;13:3114–3120. doi: 10.1021/pr401264n. PubMed DOI PMC

Rohart F, Gautier B, Singh A, Cao K-AL. mixOmics: An R package for ‘omics feature selection and multiple data integration. PLoS Comput. Biol. 2017;13:e1005752. doi: 10.1371/journal.pcbi.1005752. PubMed DOI PMC

Pavelka N, et al. A power law global error model for the identification of differentially expressed genes in microarray data. BMC Bioinform. 2004;5:203. doi: 10.1186/1471-2105-5-203. PubMed DOI PMC

Wickham H. Ggplot2: Elegant Graphics for Data Analysis. Springer; 2016.

Wu T, et al. clusterProfiler 4.0: A universal enrichment tool for interpreting omics data. The Innovation. 2021;2:100141. doi: 10.1016/j.xinn.2021.100141. PubMed DOI PMC

Matějková T, Dodoková A, Kreisinger J, Stopka P, Stopková R. Microbial, proteomic, and metabolomic profiling of the estrous cycle in wild house mice. Microbiol. Spectr. 2024 doi: 10.1128/spectrum.02037-23. PubMed DOI PMC

Grande G, et al. Proteomic characterization of the qualitative and quantitative differences in cervical mucus composition during the menstrual cycle. Mol. Biosyst. 2015;11:1717–1725. doi: 10.1039/C5MB00071H. PubMed DOI

Manstein DJ, Meiring JCM, Hardeman EC, Gunning PW. Actin–tropomyosin distribution in non-muscle cells. J. Muscle Res. Cell Motil. 2020;41:11–22. doi: 10.1007/s10974-019-09514-0. PubMed DOI PMC

Xiao S, et al. Differential gene expression profiling of mouse uterine luminal epithelium during periimplantation. Reprod. Sci. 2014;21:351–362. doi: 10.1177/1933719113497287. PubMed DOI PMC

Karantza V. Keratins in health and cancer: More than mere epithelial cell markers. Oncogene. 2011;30:127–138. doi: 10.1038/onc.2010.456. PubMed DOI PMC

Walczak J, Bocian S, Trziszka T, Buszewski B. Hyphenated analytical methods in determination of biologically active compounds in hen’s eggs. Crit. Rev. Anal. Chem. 2016;46:201–212. doi: 10.1080/10408347.2015.1023428. PubMed DOI

Bílková B, et al. Domestic fowl breed variation in egg white protein expression: Application of proteomics and transcriptomics. J. Agric. Food Chem. 2018;66:11854–11863. doi: 10.1021/acs.jafc.8b03099. PubMed DOI

Da Silva M, et al. The family secrets of avian egg-specific ovalbumin and its related proteins Y and X. Biol. Reprod. 2015;93:71–81. doi: 10.1095/biolreprod.115.130856. PubMed DOI

Sah N, Mishra B. Regulation of egg formation in the oviduct of laying hen. World’s Poult. Sci. J. 2018;74:509–522. doi: 10.1017/S0043933918000442. DOI

Bourin M, et al. Transcriptomic profiling of proteases and antiproteases in the liver of sexually mature hens in relation to vitellogenesis. BMC Genom. 2012;13:457. doi: 10.1186/1471-2164-13-457. PubMed DOI PMC

Hayward A, Takahashi T, Bendena WG, Tobe SS, Hui JHL. Comparative genomic and phylogenetic analysis of vitellogenin and other large lipid transfer proteins in metazoans. FEBS Lett. 2010;584:1273–1278. doi: 10.1016/j.febslet.2010.02.056. PubMed DOI

Sun C, Zhang S. Immune-relevant and antioxidant activities of vitellogenin and yolk proteins in fish. Nutrients. 2015;7:8818–8829. doi: 10.3390/nu7105432. PubMed DOI PMC

Lu C-L, Baker RC. Characteristics of egg yolk phosvitin as an antioxidant for inhibiting metal-catalyzed phospholipid oxidations. Poult. Sci. 1986;65:2065–2070. doi: 10.3382/ps.0652065. PubMed DOI

Saunders DK, Fowler O, Smalley KN. The effects of estradiol treatment on the blood viscosity of the bullfrog Rana catesbeiana. Trans. Kansas Acad. Sci. 2000;1903(103):38–45. doi: 10.2307/3627934. DOI

Schmoll T, Rudolfsen G, Schielzeth H, Kleven O. Sperm velocity in a promiscuous bird across experimental media of different viscosities. Proc. R. Soc. B Biol. Sci. 2020;287:20201031. doi: 10.1098/rspb.2020.1031. PubMed DOI PMC

Duggavathi R, et al. The fatty acid binding protein 6 gene (Fabp6) is expressed in murine granulosa cells and is involved in ovulatory response to superstimulation. J. Reprod. Dev. 2015;61:237–240. doi: 10.1262/jrd.2014-139. PubMed DOI PMC

Barile M, Giancaspero TA, Leone P, Galluccio M, Indiveri C. Riboflavin transport and metabolism in humans. J. Inherit. Metab. Dis. 2016;39:545–557. doi: 10.1007/s10545-016-9950-0. PubMed DOI

Kuang W, et al. SLC22A14 is a mitochondrial riboflavin transporter required for sperm oxidative phosphorylation and male fertility. Cell Rep. 2021;35:109025. doi: 10.1016/j.celrep.2021.109025. PubMed DOI PMC

Krisfalusi M, Miki K, Magyar PL, O’Brien DA. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol. Reprod. 2006;75:270–278. doi: 10.1095/biolreprod.105.049684. PubMed DOI

Tang J, et al. Dietary riboflavin supplementation improve the growth performance and antioxidant status of starter white Pekin ducks fed a corn–soybean meal diets. Livest. Sci. 2014;170:131–136. doi: 10.1016/j.livsci.2014.10.016. DOI

Saedisomeolia, A. & Ashoori, M. Riboflavin in human health: A review of current evidences. in Advances in Food and Nutrition Research vol. 83, 57–81 (Elsevier, 2018). PubMed

Lee RK-K, et al. Expression of cystatin C in the female reproductive tract and its effect on human sperm capacitation. Reprod. Biol. Endocrinol. 2018;16:1–10. doi: 10.1186/s12958-018-0327-0. PubMed DOI PMC

Li S-H, et al. Serine protease inhibitor SERPINE2 reversibly modulates murine sperm capacitation. Int. J. Mol. Sci. 2018;19:1520. doi: 10.3390/ijms19051520. PubMed DOI PMC

Surai PF, et al. Polyunsaturated fatty acids, lipid peroxidation and antioxidant protection in avian semen. Asian-Australas. J. Anim. Sci. 2001;14:1024–1050. doi: 10.5713/ajas.2001.1024. DOI

Kiyozumi D, Ikawa M. Proteolysis in reproduction: Lessons from gene-modified organism studies. Front. Endocrinol. 2022;13:87637. doi: 10.3389/fendo.2022.876370. PubMed DOI PMC

Mine Y, Kovacs-Nolan J. New insights in biologically active proteins and peptides derived from hen egg. World’s Poult. Sci. J. 2006;62:87–96. doi: 10.1079/WPS200586. DOI

Poiani A, Wilks C. Sexually transmitted diseases: A possible cost of promiscuity in birds? The Auk. 2000;117:1061–1065. doi: 10.1093/auk/117.4.1061. DOI

Perez-Riverol Y, et al. The PRIDE database resources in 2022: A hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 2022;50:D543–D552. doi: 10.1093/nar/gkab1038. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace