The evolution of centriole degradation in mouse sperm.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
02 Jan 2024
02 Jan 2024
Historique:
received:
07
03
2023
accepted:
12
12
2023
medline:
4
1
2024
pubmed:
4
1
2024
entrez:
3
1
2024
Statut:
epublish
Résumé
Centrioles are subcellular organelles found at the cilia base with an evolutionarily conserved structure and a shock absorber-like function. In sperm, centrioles are found at the flagellum base and are essential for embryo development in basal animals. Yet, sperm centrioles have evolved diverse forms, sometimes acting like a transmission system, as in cattle, and sometimes becoming dispensable, as in house mice. How the essential sperm centriole evolved to become dispensable in some organisms is unclear. Here, we test the hypothesis that this transition occurred through a cascade of evolutionary changes to the proteins, structure, and function of sperm centrioles and was possibly driven by sperm competition. We found that the final steps in this cascade are associated with a change in the primary structure of the centriolar inner scaffold protein FAM161A in rodents. This information provides the first insight into the molecular mechanisms and adaptive evolution underlying a major evolutionary transition within the internal structure of the mammalian sperm neck.
Identifiants
pubmed: 38168044
doi: 10.1038/s41467-023-44411-8
pii: 10.1038/s41467-023-44411-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
117Subventions
Organisme : United States Department of Agriculture | Agricultural Research Service (USDA Agricultural Research Service)
ID : OHOW-2020-02790
Informations de copyright
© 2024. The Author(s).
Références
Azimzadeh, J. Evolution of the centrosome, from the periphery to the center. Curr. Opin. Struct. Biol. 66, 96–103 (2021).
pubmed: 33242728
doi: 10.1016/j.sbi.2020.10.020
Winey, M. & O’Toole, E. Centriole structure. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130457 (2014).
pubmed: 25047611
pmcid: 4113101
doi: 10.1098/rstb.2013.0457
Junker, A. D. et al. Basal bodies bend in response to ciliary forces. Mol. Biol. Cell 33, ar146 (2022).
pubmed: 36287828
pmcid: 9727800
doi: 10.1091/mbc.E22-10-0468-T
Avidor-Reiss, T. & Fishman, E. L. It takes two (centrioles) to tango. Reproduction 157, R33–R51 (2019).
pubmed: 30496124
doi: 10.1530/REP-18-0350
Parker, G. A. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525–567 (1970).
doi: 10.1111/j.1469-185X.1970.tb01176.x
Birkhead, T. R. & Hunter, F. M. Mechanisms of sperm competition. Trends Ecol. Evol. 5, 48–52 (1990).
pubmed: 21232320
doi: 10.1016/0169-5347(90)90047-H
Humphries, S., Evans, J. P. & Simmons, L. W. Sperm competition: linking form to function. BMC Evol. Biol. 8, 319 (2008).
pubmed: 19032741
pmcid: 2632676
doi: 10.1186/1471-2148-8-319
Ferreira, A. & Dolder, H. Sperm ultrastructure and spermatogenesis in the lizard, Tropidurus itambere. Biocell 27, 353–362 (2003).
pubmed: 15002752
doi: 10.32604/biocell.2003.27.353
Yabe, T., Ge, X. & Pelegri, F. The zebrafish maternal-effect gene cellular atoll encodes the centriolar component sas-6 and defects in its paternal function promote whole genome duplication. Dev. Biol. 312, 44–60 (2007).
pubmed: 17950723
pmcid: 2693064
doi: 10.1016/j.ydbio.2007.08.054
Hao, S. L. & Zhang, Y. P. Ultrastructure of the spermatozoon of the Chinese water snake, Myrrophis (Enhydris) chinensis (Reptilia: Homalopsidae). Eur. Zool. J. 85, 349–361 (2018).
doi: 10.1080/24750263.2018.1506515
Hess, R. A., Thurston, R. J. & Gist, D. H. Ultrastructure of the turtle spermatozoon. Anat. Rec. 229, 473–481 (1991).
pubmed: 2048751
doi: 10.1002/ar.1092290406
Jamieson, B. G. M. in Reproductive Biology and Phylogeny of Birds: Part A Vol. 6A (ed Jamieson, B. G. M.) Ch. 8, 349–561 (Science Publishers, Inc., 2007).
Khanal, S. et al. A dynamic basal complex modulates mammalian sperm movement. Nat. Commun. 12, 3808 (2021).
pubmed: 34155206
pmcid: 8217517
doi: 10.1038/s41467-021-24011-0
Kai, Y., Kawano, H. & Yamashita, N. First mitotic spindle formation is led by sperm centrosome-dependent MTOCs in humans. Reproduction 161, V19–V22 (2021).
pubmed: 33843613
doi: 10.1530/REP-21-0061
Amargant, F. et al. The human sperm basal body is a complex centrosome important for embryo preimplantation development. Mol. Hum. Reprod. 27, gaab062 (2021).
pubmed: 34581808
pmcid: 8561016
doi: 10.1093/molehr/gaab062
Sutovsky, P. & Schatten, G. Paternal contributions to the mammalian zygote: fertilization after sperm-egg fusion. Int Rev. Cytol. 195, 1–65 (2000).
pubmed: 10603574
Uzbekov, R. et al. Centrosome formation in the bovine early embryo. bioRxiv, (2023). 2022.2011.2029.517493.
Manandhar, G., Simerly, C., Salisbury, J. L. & Schatten, G. Centriole and centrin degeneration during mouse spermiogenesis. Cell Motil. Cytoskelet. 43, 137–144 (1999).
doi: 10.1002/(SICI)1097-0169(1999)43:2<137::AID-CM5>3.0.CO;2-7
Yan, W. et al. Birth of mice after intracytoplasmic injection of single purified sperm nuclei and detection of messenger RNAs and MicroRNAs in the sperm nuclei. Biol. Reprod. 78, 896–902 (2008).
pubmed: 18256326
doi: 10.1095/biolreprod.107.067033
Kuretake, S., Kimura, Y., Hoshi, K. & Yanagimachi, R. Fertilization and development of mouse oocytes injected with isolated sperm heads. Biol. Reprod. 55, 789–795 (1996).
pubmed: 8879491
doi: 10.1095/biolreprod55.4.789
Yamauchi, Y., Yanagimachi, R. & Horiuchi, T. Full-term development of golden hamster oocytes following intracytoplasmic sperm head injection. Biol. Reprod. 67, 534–539 (2002).
pubmed: 12135892
doi: 10.1095/biolreprod67.2.534
Gueth-Hallonet, C. et al. gamma-Tubulin is present in acentriolar MTOCs during early mouse development. J. Cell Sci. 105, 157–166 (1993).
pubmed: 8360270
doi: 10.1242/jcs.105.1.157
David, A. et al. Lack of centrioles and primary cilia in STIL(-/-) mouse embryos. Cell Cycle 13, 2859–2868 (2014).
pubmed: 25486474
pmcid: 4615128
doi: 10.4161/15384101.2014.946830
Manandhar, G., Sutovsky, P., Joshi, H. C., Stearns, T. & Schatten, G. Centrosome reduction during mouse spermiogenesis. Dev. Biol. 203, 424–434 (1998).
pubmed: 9808791
doi: 10.1006/dbio.1998.8947
Courtois, A., Schuh, M., Ellenberg, J. & Hiiragi, T. The transition from meiotic to mitotic spindle assembly is gradual during early mammalian development. J. Cell Biol. 198, 357–370 (2012).
pubmed: 22851319
pmcid: 3413348
doi: 10.1083/jcb.201202135
Howe, K. & FitzHarris, G. A non-canonical mode of microtubule organization operates throughout pre-implantation development in mouse. Cell Cycle 12, 1616–1624 (2013).
pubmed: 23624836
pmcid: 3680541
doi: 10.4161/cc.24755
Pomp, O. et al. A monoastral mitotic spindle determines lineage fate and position in the mouse embryo. Nat. Cell Biol. 24, 155–167 (2022).
pubmed: 35102267
doi: 10.1038/s41556-021-00826-3
Parker, G. A. The sexual cascade and the rise of pre-ejaculatory (Darwinian) sexual selection, sex roles, and sexual conflict. Cold Spring Harb. Perspect. Biol. 6, a017509 (2014).
pubmed: 25147177
pmcid: 4176012
doi: 10.1101/cshperspect.a017509
Lüpold, S., de Boer, R. A., Evans, J. P., Tomkins, J. L. & Fitzpatrick, J. L. How sperm competition shapes the evolution of testes and sperm: a meta-analysis. Philos. Trans. R. Soc. B 375, 20200064 (2020).
doi: 10.1098/rstb.2020.0064
Mokos, J., Scheuring, I., Liker, A., Freckleton, R. P. & Székely, T. Degree of anisogamy is unrelated to the intensity of sexual selection. Sci. Rep. 11, 1–11 (2021).
Schill, D. J., LaBar, G. W., Mamer, E. R. J. M. & Meyer, K. A. Sex ratio, fecundity, and models predicting length at sexual maturity of redband trout in Idaho desert streams. North Am. J. Fish. Manag. 30, 1352–1363 (2010).
doi: 10.1577/M10-021.1
Rowley, A. G., Daly-Engel, T. S. & Fitzpatrick, J. L. Testes size increases with sperm competition risk and intensity in bony fish and sharks. Behav. Ecol. 30, 364–371 (2019).
doi: 10.1093/beheco/ary174
Fisher, H. S., Jacobs-Palmer, E., Lassance, J. M. & Hoekstra, H. E. The genetic basis and fitness consequences of sperm midpiece size in deer mice. Nat. Commun. 7, 13652 (2016).
pubmed: 27910854
pmcid: 5146288
doi: 10.1038/ncomms13652
Gomendio, M. & Roldan, E. R. Sperm competition influences sperm size in mammals. Proc. Biol. Sci. 243, 181–185 (1991).
pubmed: 1675796
doi: 10.1098/rspb.1991.0029
Joly, D., Korol, A. & Nevo, E. Sperm size evolution in Drosophila: inter- and intraspecific analysis. Genetica 120, 233–244 (2004).
pubmed: 15088661
doi: 10.1023/B:GENE.0000017644.63389.57
Kahrl, A. F., Snook, R. R. & Fitzpatrick, J. L. Fertilization mode drives sperm length evolution across the animal tree of life. Nat. Ecol. Evol. 5, 1153–1164 (2021).
pubmed: 34155385
doi: 10.1038/s41559-021-01488-y
Turner, K., Solanki, N., Salouha, H. O. & Avidor-Reiss, T. Atypical centriolar composition correlates with internal fertilization in fish. Cells 11, 758 (2022).
pubmed: 35269380
pmcid: 8909020
doi: 10.3390/cells11050758
Fishman, E. L. et al. Atypical centrioles are present in Tribolium sperm. Open Biol. 7, 160334 (2017).
pubmed: 28298310
pmcid: 5376708
doi: 10.1098/rsob.160334
Khire, A. et al. Centriole remodeling during spermiogenesis in Drosophila. Curr. Biol. 26, 3183–3189 (2016).
pubmed: 28094036
pmcid: 5245371
doi: 10.1016/j.cub.2016.07.006
Tung, C. K. & Suarez, S. S. Co-adaptation of physical attributes of the mammalian female reproductive tract and sperm to facilitate fertilization. Cells 10, 1297 (2021).
pubmed: 34073739
pmcid: 8225031
doi: 10.3390/cells10061297
Cavazza, T. et al. Parental genome unification is highly error-prone in mammalian embryos. Cell 184, 2860–2877.e2822 (2021).
pubmed: 33964210
pmcid: 8162515
doi: 10.1016/j.cell.2021.04.013
Shin, T.-Y., Noguchi, Y., Yamamoto, Y., MOCHIDA, K. & OGURA, A. Microtubule organization in hamster oocytes after fertilization with mature spermatozoa and round spermatids. J. Reprod. Dev. 44, 185–189 (1998).
doi: 10.1262/jrd.44.185
Woolley, D. M. & Fawcett, D. W. The degeneration and disappearance of the centrioles during the development of the rat spermatozoon. Anat. Rec. 177, 289–301 (1973).
pubmed: 4356969
doi: 10.1002/ar.1091770209
Fawcett, D. W. The mammalian spermatozoon. Dev. Biol. 44, 394–436 (1975).
pubmed: 805734
doi: 10.1016/0012-1606(75)90411-X
Schatten, H., Schatten, G., Mazia, D., Balczon, R. & Simerly, C. Behavior of centrosomes during fertilization and cell division in mouse oocytes and in sea urchin eggs. Proc. Natl Acad. Sci. USA 83, 105–109 (1986).
pubmed: 2417231
pmcid: 322800
doi: 10.1073/pnas.83.1.105
Simerly, C. R., Hecht, N. B., Goldberg, E. & Schatten, G. Tracing the incorporation of the sperm tail in the mouse zygote and early embryo using an anti-testicular alpha-tubulin antibody. Dev. Biol. 158, 536–548 (1993).
pubmed: 8344468
doi: 10.1006/dbio.1993.1211
Coelho, P. A. et al. Spindle formation in the mouse embryo requires Plk4 in the absence of centrioles. Dev. Cell 27, 586–597 (2013).
pubmed: 24268700
pmcid: 3898710
doi: 10.1016/j.devcel.2013.09.029
Bangs, F. K., Schrode, N., Hadjantonakis, A. K. & Anderson, K. V. Lineage specificity of primary cilia in the mouse embryo. Nat. Cell Biol. 17, 113–122 (2015).
pubmed: 25599390
pmcid: 4406239
doi: 10.1038/ncb3091
Schatten, G., Simerly, C. & Schatten, H. Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc. Natl Acad. Sci. USA 82, 4152–4156 (1985).
pubmed: 3889922
pmcid: 397953
doi: 10.1073/pnas.82.12.4152
Calarco, P. G. Centrosome precursors in the acentriolar mouse oocyte. Microsc Res. Tech. 49, 428-434 (2000).
Clift, D. & Schuh, M. A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes. Nat. Commun. 6, 7217 (2015).
pubmed: 26147444
doi: 10.1038/ncomms8217
Zenker, J. et al. A microtubule-organizing center directing intracellular transport in the early mouse embryo. Science 357, 925–928 (2017).
pubmed: 28860385
doi: 10.1126/science.aam9335
Jin, Y. X. et al. Cat fertilization by mouse sperm injection. Zygote 20, 371–378 (2012).
pubmed: 21791165
doi: 10.1017/S0967199411000451
Fishman, E.L., et al. 2021. The Typical and Atypical Centrioles and Their Potential Roles in the Sperm and Embryo. 85–120 (Springer International Publishing, 2021).
Palacios Martinez, S., Greaney, J. & Zenker, J. Beyond the centrosome: the mystery of microtubule organising centres across mammalian preimplantation embryos. Curr. Opin. Cell Biol. 77, 102114 (2022).
pubmed: 35841745
doi: 10.1016/j.ceb.2022.102114
Leung, M. R. et al. The multi-scale architecture of mammalian sperm flagella and implications for ciliary motility. EMBO J. 40, e107410 (2021).
pubmed: 33694216
pmcid: 8013824
doi: 10.15252/embj.2020107410
Breslow, D. K. & Holland, A. J. Mechanism and regulation of centriole and cilium biogenesis. Annu Rev. Biochem 88, 691–724 (2019).
pubmed: 30601682
pmcid: 6588485
doi: 10.1146/annurev-biochem-013118-111153
Greenan, G. A., Keszthelyi, B., Vale, R. D. & Agard, D. A. Insights into centriole geometry revealed by cryotomography of doublet and triplet centrioles. eLife 7, e36851 (2018).
pubmed: 30080137
pmcid: 6110610
doi: 10.7554/eLife.36851
Ross, B. D. et al. Stepwise evolution of essential centromere function in a Drosophila Neogene. Science 340, 1211–1214 (2013).
pubmed: 23744945
pmcid: 4119826
doi: 10.1126/science.1234393
Finseth, F. R., Dong, Y., Saunders, A. & Fishman, L. Duplication and adaptive evolution of a key centromeric protein in mimulus, a genus with female meiotic drive. Mol. Biol. Evol. 32, 2694–2706 (2015).
pubmed: 26104011
doi: 10.1093/molbev/msv145
Henikoff, S., Thakur, J., Kasinathan, S. & Talbert, P. B. in Cold Spring Harbor symposia on quantitative biology. 71–82 (Cold Spring Harbor Laboratory Press, 2017).
Henikoff, S., Ahmad, K. & Malik, H. S. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293, 1098–1102 (2001).
pubmed: 11498581
doi: 10.1126/science.1062939
Fishman, E. L. et al. A novel atypical sperm centriole is functional during human fertilization. Nat. Commun. 9, 2210 (2018).
pubmed: 29880810
pmcid: 5992222
doi: 10.1038/s41467-018-04678-8
Le Guennec, M. et al. A helical inner scaffold provides a structural basis for centriole cohesion. Sci. Adv. 6, eaaz4137 (2020).
pubmed: 32110738
pmcid: 7021493
doi: 10.1126/sciadv.aaz4137
Steib, E. et al. WDR90 is a centriolar microtubule wall protein important for centriole architecture integrity. eLife 9, e57205 (2020).
pubmed: 32946374
pmcid: 7500955
doi: 10.7554/eLife.57205
Manandhar, G., Simerly, C. & Schatten, G. Highly degenerated distal centrioles in rhesus and human spermatozoa. Hum. Reprod. 15, 256–263 (2000).
pubmed: 10655294
doi: 10.1093/humrep/15.2.256
Xu, B. et al. TSKS concentrates in spermatid centrioles during flagellogenesis. Dev. Biol. 319, 201–210 (2008).
pubmed: 18495105
pmcid: 2670488
doi: 10.1016/j.ydbio.2008.03.043
Gordon, M. & Bensch, K. G. Cytochemical differentiation of the guinea pig sperm flagellum with phosphotungstic acid. J. Ultrastruct. Res. 24, 33–50 (1968).
pubmed: 4176337
doi: 10.1016/S0022-5320(68)80015-2
Fawcett, D. W. The anatomy of the mammalian spermatozoon with particular reference to the guinea pig. Z. Zellforsch. Mikros. Anat. 67, 279–296 (1965).
doi: 10.1007/BF00339376
Healey, P. & Weir, B. J. Changes in the ultrastructure of chinchilla spermatozoa in different diluents. J. Reprod. Fertil. 21, 191–193 (1970).
pubmed: 4905089
doi: 10.1530/jrf.0.0210191
Soley, J. T. A comparative overview of the sperm centriolar complex in mammals and birds: Variations on a theme. Anim. Reprod. Sci. 169, 14–23 (2016).
pubmed: 26907939
doi: 10.1016/j.anireprosci.2016.02.006
Arroyo, M. A. M. et al. Ultrastructure of spermatogenesis and spermatozoa in agoutis during sexual development. Reprod. Fertil. Dev. 29, 383–393 (2017).
pubmed: 26336816
doi: 10.1071/RD14442
Santos, P. R. et al. Ultrastructure of spermatogenesis in Spix’s yellow-toothed cavy (Galea spixii). Reproduction 147, 13–19 (2014).
pubmed: 24101585
doi: 10.1530/REP-13-0452
Van Der Horst, G., Maree, L., Kotze, S. H. & O’Riain, M. J. Sperm structure and motility in the eusocial naked mole-rat, Heterocephalus glaber: a case of degenerative orthogenesis in the absence of sperm competition? BMC Evol. Biol. 11, 351 (2011).
pubmed: 22142177
pmcid: 3247228
doi: 10.1186/1471-2148-11-351
Lee, J.-H. & Park, K.-R. Fine structure of sperm in the Korea squirrel, Tamias sibiricus. Appl. Microscopy 41, 99–107 (2011).
Hruban, Z., Martan, J. & Aschenbrenner, I. Polarized cylindrical body in the epididymis of the flying squirrel. J. Morphol. 135, 87–97 (1971).
pubmed: 5137696
doi: 10.1002/jmor.1051350106
Franklin, L. E., Barros, C. & Fussell, E. N. The acrosomal region and the acrosome reaction in sperm of the golden hamster. Biol. Reprod. 3, 180–200 (1970).
pubmed: 5522851
doi: 10.1093/biolreprod/3.2.180
Yanagimachi, R., Kamiguchi, Y., Sugawara, S. & Mikamo, K. Gametes and fertilization in the Chinese hamster. Gamete Res. 8, 97–117 (1983).
doi: 10.1002/mrd.1120080202
Garcia Lorenzana, M., Lopez Wilchis, R. & Vazquez Nin, G. Basic aspects of the fine structure of Peromyscus winkelmamzi spermatozoa (Rodentia: Cricetidae). Biblioteca 4 (1998).
Lee, J.-H. & Mori, T. Ultrastructural observations on the sperm of two Apodemus species, Apodemus agrarius coreae and Apodemus speciosus peninsulae, in Korea. (2006).
Chakraborty, J. Neck region of gerbil spermatozoa. Gamete Res. 2, 25–34 (1979).
doi: 10.1002/mrd.1120020104
Steppan, S. J. & Schenk, J. J. Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates. PLoS One 12, e0183070 (2017).
pubmed: 28813483
pmcid: 5559066
doi: 10.1371/journal.pone.0183070
Li, Y. Z. et al. Biallelic mutations in spermatogenesis and centriole-associated 1 like (SPATC1L) cause acephalic spermatozoa syndrome and male infertility. Asian J. Androl. 24, 67–72 (2022).
pubmed: 34213489
doi: 10.4103/aja.aja_56_21
Temple-Smith, P., Ravichandran, A. & Horta, F. Sperm: comparative vertebrate. Encycl. Reprod. 2, 210–220 (2018).
doi: 10.1016/B978-0-12-809633-8.20558-X
Hamasaki, M., Wakimoto, M., Maehara, T. & Matsuo, H. Three-dimensional structures of the neck region of the hamster spermatozoa in the caudal epididymis. Arch. Histol. Cytol. 57, 59–65 (1994).
pubmed: 8198835
doi: 10.1679/aohc.57.59
Breed, W. G., Leigh, C. M., Aplin, K. P., Shahin, A. A. & Avenant, N. L. Morphological diversity and evolution of the spermatozoon in the mouse-related clade of rodents. J. Morphol. 275, 540–547 (2014).
pubmed: 24338943
doi: 10.1002/jmor.20236
Varea Sanchez, M., Bastir, M. & Roldan, E. R. Geometric morphometrics of rodent sperm head shape. PLoS One 8, e80607 (2013).
pubmed: 24312234
pmcid: 3842927
doi: 10.1371/journal.pone.0080607
Baker, M. A. et al. Head and flagella subcompartmental proteomic analysis of human spermatozoa. Proteomics 13, 61–74 (2013).
pubmed: 23161668
doi: 10.1002/pmic.201200350
Baker, M. A. et al. Identification of gene products present in Triton X-100 soluble and insoluble fractions of human spermatozoa lysates using LC-MS/MS analysis. Proteom. Clin. Appl 1, 524–532 (2007).
doi: 10.1002/prca.200601013
Amaral, A. et al. Human sperm tail proteome suggests new endogenous metabolic pathways. Mol. Cell Proteom. 12, 330–342 (2013).
doi: 10.1074/mcp.M112.020552
Wang, G. et al. In-depth proteomic analysis of the human sperm reveals complex protein compositions. J. Proteom. 79, 114–122 (2013).
doi: 10.1016/j.jprot.2012.12.008
Alves-Cruzeiro, J. M., Nogales-Cadenas, R. & Pascual-Montano, A. D. CentrosomeDB: a new generation of the centrosomal proteins database for Human and Drosophila melanogaster. Nucleic Acids Res. 42, D430–436 (2014).
pubmed: 24270791
doi: 10.1093/nar/gkt1126
Thybert, D. et al. Repeat associated mechanisms of genome evolution and function revealed by the Mus caroli and Mus pahari genomes. Genome Res 28, 448–459 (2018).
pubmed: 29563166
pmcid: 5880236
doi: 10.1101/gr.234096.117
Clark, N. L., Aagaard, J. E. & Swanson, W. J. Evolution of reproductive proteins from animals and plants. Reproduction 131, 11–22 (2006).
pubmed: 16388004
doi: 10.1530/rep.1.00357
Swanson, W. J. & Vacquier, V. D. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3, 137–144 (2002).
pubmed: 11836507
doi: 10.1038/nrg733
Gozashti, L., Corbett-Detig, R. & Roy, S. W. Evolutionary rates of testes-expressed genes differ between monogamous and promiscuous Peromyscus species. bioRxiv, 2021.2004.2021.440792 (2021). https://doi.org/10.1101/2021.04.21.440792
Luke, L., Tourmente, M. & Roldan, E. R. Sexual selection of protamine 1 in mammals. Mol. Biol. Evol. 33, 174–184 (2016).
pubmed: 26429923
doi: 10.1093/molbev/msv209
Toll-Riera, M., Laurie, S. & Alba, M. M. Lineage-specific variation in intensity of natural selection in mammals. Mol. Biol. Evol. 28, 383–398 (2011).
pubmed: 20688808
doi: 10.1093/molbev/msq206
Bazzi, H. & Anderson, K. V. Centrioles in the mouse: cilia and beyond. Cell Cycle 13, 2809 (2014).
pubmed: 25486466
pmcid: 4614153
doi: 10.4161/15384101.2014.954450
Zach, F. & Stohr, H. FAM161A, a novel centrosomal-ciliary protein implicated in autosomal recessive retinitis pigmentosa. Adv. Exp. Med Biol. 801, 185–190 (2014).
pubmed: 24664697
doi: 10.1007/978-1-4614-3209-8_24
Bandah-Rozenfeld, D. et al. Homozygosity mapping reveals null mutations in FAM161A as a cause of autosomal-recessive retinitis pigmentosa. Am. J. Hum. Genet. 87, 382–391 (2010).
pubmed: 20705279
pmcid: 2933343
doi: 10.1016/j.ajhg.2010.07.022
Langmann, T. et al. Nonsense mutations in FAM161A cause RP28-associated recessive retinitis pigmentosa. Am. J. Hum. Genet 87, 376–381 (2010).
pubmed: 20705278
pmcid: 2933350
doi: 10.1016/j.ajhg.2010.07.018
Downs, L. M. & Mellersh, C. S. An Intronic SINE insertion in FAM161A that causes exon-skipping is associated with progressive retinal atrophy in Tibetan Spaniels and Tibetan Terriers. PLoS One 9, e93990 (2014).
pubmed: 24705771
pmcid: 3976383
doi: 10.1371/journal.pone.0093990
Green, C. D. et al. A comprehensive roadmap of murine spermatogenesis defined by single-cell RNA-Seq. Dev. Cell 46, 651–667.e610 (2018).
pubmed: 30146481
pmcid: 6713459
doi: 10.1016/j.devcel.2018.07.025
Zach, F. et al. The retinitis pigmentosa 28 protein FAM161A is a novel ciliary protein involved in intermolecular protein interaction and microtubule association. Hum. Mol. Genet 21, 4573–4586 (2012).
pubmed: 22791751
doi: 10.1093/hmg/dds268
Doxsey, S. J., Stein, P., Evans, L., Calarco, P. D. & Kirschner, M. Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76, 639–650 (1994).
pubmed: 8124707
doi: 10.1016/0092-8674(94)90504-5
Azimzadeh, J. et al. hPOC5 is a centrin-binding protein required for assembly of full-length centrioles. J. Cell Biol. 185, 101–114 (2009).
pubmed: 19349582
pmcid: 2700515
doi: 10.1083/jcb.200808082
Mercey, O. et al. The connecting cilium inner scaffold provides a structural foundation that protects against retinal degeneration. PLoS Biol. 20, e3001649 (2022).
pubmed: 35709082
pmcid: 9202906
doi: 10.1371/journal.pbio.3001649
Roosing, S. et al. Disruption of the basal body protein POC1B results in autosomal-recessive cone-rod dystrophy. Am. J. Hum. Genet 95, 131–142 (2014).
pubmed: 25018096
pmcid: 4129401
doi: 10.1016/j.ajhg.2014.06.012
Zamboni, L. & Stefanini, M. The fine structure of the neck of mammalian spermatozoa. Anat. Rec. 169, 155–172 (1971).
pubmed: 5544616
doi: 10.1002/ar.1091690203
Garanina, A. S. et al. The centriolar adjunct(-)appearance and disassembly in spermiogenesis and the potential impact on fertility. Cells 8, 180 (2019).
pubmed: 30791486
pmcid: 6406449
doi: 10.3390/cells8020180
Manandhar, G., Schatten, H. & Sutovsky, P. Centrosome reduction during gametogenesis and its significance. Biol. Reprod. 72, 2–13 (2005).
pubmed: 15385423
doi: 10.1095/biolreprod.104.031245
Roldan, E. R. S. Sperm competition and the evolution of sperm form and function in mammals. Reprod. Domest. Anim. 54, 14–21 (2019).
pubmed: 31625240
doi: 10.1111/rda.13552
Avidor-Reiss, T., Ha, A. & Basiri, M. L. Transition zone migration: a mechanism for cytoplasmic ciliogenesis and postaxonemal centriole elongation. Cold Spring Harb. Perspect. Biol. 9, a028142 (2017).
pubmed: 28108487
pmcid: 5538411
doi: 10.1101/cshperspect.a028142
Wu, B., Gao, H., Liu, C. & Li, W. The coupling apparatus of the sperm head and taildagger. Biol. Reprod. 102, 988–998 (2020).
pubmed: 31995163
doi: 10.1093/biolre/ioaa016
Tapia Contreras, C. & Hoyer-Fender, S. The transformation of the centrosome into the basal body: similarities and dissimilarities between somatic and male germ cells and their relevance for male fertility. Cells 10, 2266 (2021).
pubmed: 34571916
pmcid: 8471410
doi: 10.3390/cells10092266
Jamieson, B. G. Fish evolution and systematics: evidence from spermatozoa: with a survey of lophophorate, echinoderm and protochordate sperm and an account of gamete cryopreservation (Cambridge University Press, 1991).
Avidor-Reiss, T. Rapid evolution of sperm produces diverse centriole structures that reveal the most rudimentary structure needed for function. Cells 7, 67 (2018).
pubmed: 29949922
pmcid: 6071034
doi: 10.3390/cells7070067
Steppan, S., Adkins, R. & Anderson, J. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst. Biol. 53, 533–553 (2004).
pubmed: 15371245
doi: 10.1080/10635150490468701
Lemaitre, J. F., Gaillard, J. M. & Ramm, S. A. The hidden ageing costs of sperm competition. Ecol. Lett. 23, 1573–1588 (2020).
pubmed: 32906225
doi: 10.1111/ele.13593
Lüpold, S. & Pitnick, S. Sperm form and function: what do we know about the role of sexual selection? Reproduction 155, R229–R243 (2018).
pubmed: 29459400
doi: 10.1530/REP-17-0536
Avidor-Reiss, T., Achinger, L. & Uzbekov, R. The centriole’s role in miscarriages. Front Cell Dev. Biol. 10, 864692 (2022).
pubmed: 35300410
pmcid: 8922021
doi: 10.3389/fcell.2022.864692
Kumar, D. & Reiter, J. How the centriole builds its cilium: of mothers, daughters, and the acquisition of appendages. Curr. Opin. Struct. Biol. 66, 41–48 (2021).
pubmed: 33160100
doi: 10.1016/j.sbi.2020.09.006
Phillips, D. M. Giant centriole formation in Sciara. J. Cell Biol. 33, 73–92 (1967).
pubmed: 6068031
pmcid: 2107291
doi: 10.1083/jcb.33.1.73
Avidor-Reiss, T. & Turner, K. The evolution of centriole structure: heterochrony, neoteny, and hypermorphosis. Results Probl. Cell Differ. 67, 3–15 (2019).
pubmed: 31435789
pmcid: 7576685
doi: 10.1007/978-3-030-23173-6_1
Avidor-Reiss, T., Carr, A. & Fishman, E. L. The sperm centrioles. Mol. Cell Endocrinol. 518, 110987 (2020).
pubmed: 32810575
pmcid: 7606549
doi: 10.1016/j.mce.2020.110987
Rawe, V. Y. et al. A pathology of the sperm centriole responsible for defective sperm aster formation, syngamy and cleavage. Hum. Reprod. 17, 2344–2349 (2002).
pubmed: 12202423
doi: 10.1093/humrep/17.9.2344
Scheffler, K. et al. Two mechanisms drive pronuclear migration in mouse zygotes. Nat. Commun. 12, 841 (2021).
pubmed: 33547291
pmcid: 7864974
doi: 10.1038/s41467-021-21020-x
Hook, K. A., Wilke, L. M. & Fisher, H. S. Apical sperm hook morphology is linked to sperm swimming performance and sperm aggregation in Peromyscus mice. Cells 10, 2279 (2021).
pubmed: 34571928
pmcid: 8471468
doi: 10.3390/cells10092279
Birkhead, T., Møller, A. & Sutherland, W. Why do females make it so difficult for males to fertilize their eggs? J. Theor. Biol. 161, 51–60 (1993).
doi: 10.1006/jtbi.1993.1039
Roldan, E. R., Gomendio, M. & Vitullo, A. D. The evolution of eutherian spermatozoa and underlying selective forces: female selection and sperm competition. Biol. Rev. Camb. Philos. Soc. 67, 551–593 (1992).
pubmed: 1463811
doi: 10.1111/j.1469-185X.1992.tb01193.x
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147
pmcid: 390337
doi: 10.1093/nar/gkh340
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).
pubmed: 28481363
pmcid: 5453245
doi: 10.1038/nmeth.4285
Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).
pubmed: 22357727
pmcid: 3329765
doi: 10.1093/sysbio/sys029
Rambaut, A. University of Edinburgh, Institute of Evolutionary Biology; Edinburgh, UK: 2012. FigTree V. 1.4. Molecular Evolution, Phylogenetics and Epidemiology.
Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
pubmed: 17483113
doi: 10.1093/molbev/msm088