Section: Evolutionary Biology
Topic: Evolution, Population biology

Evolution of sperm morphology in a crustacean genus with fertilization inside an open brood pouch

10.24072/pcjournal.182 - Peer Community Journal, Volume 2 (2022), article no. e63.

Get full text PDF Peer reviewed and recommended by PCI

Sperm is the most fundamental male reproductive feature. It serves the fertilization of eggs and evolves under sexual selection. Two components of sperm are of particular interest, their number and their morphology. Mode of fertilization is believed to be a key determinant of sperm length across the animal kingdom. External fertilization, unlike internal, favors small and numerous sperm, since sperm density is thinned out in the environment. Here, we study the evolution of sperm morphology in the genus Daphnia, where fertilization occurs in a receptacle, the brood pouch, where sperm can constantly be flushed out by a water current. Based on microscopic observations of sperm morphologies mapped on a phylogeny with 15 Daphnia and 2 outgroup species, we found that despite the internal fertilization mode, Daphnia have among the smallest sperm recorded, as would be expected with external fertilization. Despite being all relatively small compared to other arthropods, sperm length diverged at least twice, once within each of the Daphnia subgenera Ctenodaphnia and Daphnia. Furthermore, species in the latter subgenus also lost the ability of cell compaction by extracellular encapsulation and have very polymorphic sperm with long, and often numerous, filopodia. We discuss the different strategies that Daphnia evolved to achieve fertilization success in the females’ brood pouch.

Published online:
DOI: 10.24072/pcjournal.182
Type: Research article
Duneau, David 1, 2; Möst, Markus 3; Ebert, Dieter 2

1 Université Toulouse 3 Paul Sabatier, CNRS, IRD; UMR5174, EDB (Laboratoire Évolution & Diversité Biologique); Toulouse, France
2 University of Basel, Department of Environmental Sciences, Zoology, Vesalgasse 1, 4051 Basel, Switzerland
3 University of Innsbruck, Department of Ecology, Technikerstrasse 25, 6020 Innsbruck, Austria
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
@article{10_24072_pcjournal_182,
     author = {Duneau, David and M\"ost, Markus and Ebert, Dieter},
     title = {Evolution of sperm morphology in a crustacean genus with fertilization inside an open brood pouch},
     journal = {Peer Community Journal},
     eid = {e63},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.182},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.182/}
}
TY  - JOUR
AU  - Duneau, David
AU  - Möst, Markus
AU  - Ebert, Dieter
TI  - Evolution of sperm morphology in a crustacean genus with fertilization inside an open brood pouch
JO  - Peer Community Journal
PY  - 2022
VL  - 2
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.182/
DO  - 10.24072/pcjournal.182
ID  - 10_24072_pcjournal_182
ER  - 
%0 Journal Article
%A Duneau, David
%A Möst, Markus
%A Ebert, Dieter
%T Evolution of sperm morphology in a crustacean genus with fertilization inside an open brood pouch
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.182/
%R 10.24072/pcjournal.182
%F 10_24072_pcjournal_182
Duneau, David; Möst, Markus; Ebert, Dieter. Evolution of sperm morphology in a crustacean genus with fertilization inside an open brood pouch. Peer Community Journal, Volume 2 (2022), article  no. e63. doi : 10.24072/pcjournal.182. https://peercommunityjournal.org/articles/10.24072/pcjournal.182/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100145

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Adamowicz, S. J.; Petrusek, A.; Colbourne, J. K.; Hebert, P. D.; Witt, J. D. The scale of divergence: A phylogenetic appraisal of intercontinental allopatric speciation in a passively dispersed freshwater zooplankton genus, Molecular Phylogenetics and Evolution, Volume 50 (2009) no. 3, pp. 423-436 | DOI

[2] Baldass, F. Entwicklung von Daphnia pulex In: Abteilung Fur Anatomie und Ontogenie der Tiere, Verlag von Gustav Fischer, Jena, Germany (1941)

[3] Benzie, J. Cladocera: The genus Daphnia (including Daphniopsis), Backhuys Publishers, Leiden, The Netherlands, 2005

[4] Birkhead, T.; Hosken, D.; Pitnick, S. Sperm biology: an evolutionary perspective, Academic Press Elsevier, 2009

[5] Chernomor, O.; von Haeseler, A.; Minh, B. Q. Terrace Aware Data Structure for Phylogenomic Inference from Supermatrices, Systematic Biology, Volume 65 (2016) no. 6, pp. 997-1008 | DOI

[6] Cornetti, L.; Fields, P. D.; Van Damme, K.; Ebert, D. A fossil-calibrated phylogenomic analysis of Daphnia and the Daphniidae, Molecular Phylogenetics and Evolution, Volume 137 (2019), pp. 250-262 | DOI

[7] Delavault, R.; Berard, J. Ultrastructural study of spermatogenesis in Daphnia magna Straus (Entomostraca, Branchiopoda, Cladocerae), Comptes Rendus Hebdomadaires des Seances de l'Academie des Sciences Serie D, Volume 278 (1974), pp. 1589-1592

[8] De Meester, L.; Vanoverbeke, J. An uncoupling of male and sexual egg production leads to reduced inbreeding in the cyclical parthenogen<i>Daphnia</i>, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 266 (1999) no. 1437, pp. 2471-2477 | DOI

[9] Deng, H.-W.; Lynch, M. Change of Genetic Architecture in Response to Sex, Genetics, Volume 143 (1996) no. 1, pp. 203-212 | DOI

[10] Duneau, D.; Altermatt, F.; Ferdy, J.-B.; Ben-Ami, F.; Ebert, D. Estimation of the propensity for sexual selection in a cyclical parthenogen, bioRxiv | DOI

[11] Duneau, D.; Luijckx, P.; Ruder, L. F.; Ebert, D. Sex-specific effects of a parasite evolving in a female-biased host population, BMC Biology, Volume 10 (2012) no. 1 | DOI

[12] Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Research, Volume 32 (2004) no. 5, pp. 1792-1797 | DOI

[13] Fitzpatrick, J. L.; Kahrl, A. F.; Snook, R. R. SpermTree, a species-level database of sperm morphology spanning the animal tree of life, Scientific Data, Volume 9 (2022) no. 1 | DOI

[14] Flössner, D. Die Haplopoda und Cladocera (ohne Bosminidae) Mitteleuropas, Backhuys Publishers, Leiden, The Netherlands, 2000

[15] Guindon, S.; Dufayard, J.-F.; Lefort, V.; Anisimova, M.; Hordijk, W.; Gascuel, O. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0, Systematic Biology, Volume 59 (2010) no. 3, pp. 307-321 | DOI

[16] Harmon, L. J.; Weir, J. T.; Brock, C. D.; Glor, R. E.; Challenger, W. GEIGER: investigating evolutionary radiations, Bioinformatics, Volume 24 (2008) no. 1, pp. 129-131 | DOI

[17] Hoang, D. T.; Chernomor, O.; von Haeseler, A.; Minh, B. Q.; Vinh, L. S. UFBoot2: Improving the Ultrafast Bootstrap Approximation, Molecular Biology and Evolution, Volume 35 (2018) no. 2, pp. 518-522 | DOI

[18] Immler, S.; Pitnick, S.; Parker, G. A.; Durrant, K. L.; Lüpold, S.; Calhim, S.; Birkhead, T. R. Resolving variation in the reproductive tradeoff between sperm size and number, Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 13, pp. 5325-5330 | DOI

[19] Kahrl, A. F.; Snook, R. R.; Fitzpatrick, J. L. Fertilization mode drives sperm length evolution across the animal tree of life, Nature Ecology &amp; Evolution, Volume 5 (2021) no. 8, pp. 1153-1164 | DOI

[20] Kalyaanamoorthy, S.; Minh, B. Q.; Wong, T. K. F.; von Haeseler, A.; Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates, Nature Methods, Volume 14 (2017) no. 6, pp. 587-589 | DOI

[21] Kishino, H.; Hasegawa, M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea, Journal of Molecular Evolution, Volume 29 (1989) no. 2, pp. 170-179 | DOI

[22] Kishino, H.; Miyata, T.; Hasegawa, M. Maximum likelihood inference of protein phylogeny and the origin of chloroplasts, Journal of Molecular Evolution, Volume 31 (1990) no. 2, pp. 151-160 | DOI

[23] Lee, D.; Nah, J. S.; Yoon, J.; Kim, W.; Rhee, K. Live observation of the oviposition process in Daphnia magna, PLOS ONE, Volume 14 (2019) no. 11 | DOI

[24] Lüpold, S.; Pitnick, S. Sperm form and function: what do we know about the role of sexual selection?, Reproduction, Volume 155 (2018) no. 5 | DOI

[25] Minh, B. Q.; Schmidt, H. A.; Chernomor, O.; Schrempf, D.; Woodhams, M. D.; von Haeseler, A.; Lanfear, R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era, Molecular Biology and Evolution, Volume 37 (2020) no. 5, pp. 1530-1534 | DOI

[26] Nguyen, L.-T.; Schmidt, H. A.; von Haeseler, A.; Minh, B. Q. IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies, Molecular Biology and Evolution, Volume 32 (2015) no. 1, pp. 268-274 | DOI

[27] Niksirat, H.; Kouba, A.; Kozák, P. Post-mating morphological changes in the spermatozoon and spermatophore wall of the crayfish Astacus leptodactylus: Insight into a non-motile spermatozoon, Animal Reproduction Science, Volume 149 (2014) no. 3-4, pp. 325-334 | DOI

[28] Paradis, E.; Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R, Bioinformatics, Volume 35 (2019) no. 3, pp. 526-528 | DOI

[29] Parker, G. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes, Journal of Theoretical Biology, Volume 96 (1982) no. 2, pp. 281-294 | DOI

[30] Pennell, M. W.; Eastman, J. M.; Slater, G. J.; Brown, J. W.; Uyeda, J. C.; FitzJohn, R. G.; Alfaro, M. E.; Harmon, L. J. geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees, Bioinformatics, Volume 30 (2014) no. 15, pp. 2216-2218 | DOI

[31] Pitnick, S.; Hosken, D. J.; Birkhead, T. R. Sperm morphological diversity, Sperm Biology, Elsevier, 2009, pp. 69-149 | DOI

[32] Popova, E. V.; Petrusek, A.; Kořínek, V.; Mergeay, J.; Bekker, E. I.; Karabanov, D. P.; Galimov, Y. R.; Neretina, T. V.; Taylor, D. J.; Kotov, A. A. Revision of the Old World Daphnia (Ctenodaphnia) similis group Cladocera: Daphniidae), Zootaxa, Volume 4161 (2016) no. 1 | DOI

[33] R Core Team R: A language and environment for statistical computing. Vienna, Austria., 2020

[34] Ramm, S. A.; Scharer, L.; Ehmcke, J.; Wistuba, J. Sperm competition and the evolution of spermatogenesis, Molecular Human Reproduction, Volume 20 (2014) no. 12, pp. 1169-1179 | DOI

[35] Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things), Methods in Ecology and Evolution, Volume 3 (2012) no. 2, pp. 217-223 | DOI

[36] Roldan, E. R. S. Sperm competition and the evolution of sperm form and function in mammals, Reproduction in Domestic Animals, Volume 54 (2019), pp. 14-21 | DOI

[37] Roulin, A. C.; Routtu, J.; Hall, M. D.; Janicke, T.; Colson, I.; Haag, C. R.; Ebert, D. Local adaptation of sex induction in a facultative sexual crustacean: insights from QTL mapping and natural populations of<i>Daphnia magna</i>, Molecular Ecology, Volume 22 (2013) no. 13, pp. 3567-3579 | DOI

[38] Seidl, M. D.; Pirow, R.; Paul, R. J. Water fleas (Daphnia magna) provide a separate ventilatory mechanism for their brood, Zoology, Volume 105 (2002) no. 1, pp. 15-23 | DOI

[39] Shimodaira, H. An Approximately Unbiased Test of Phylogenetic Tree Selection, Systematic Biology, Volume 51 (2002) no. 3, pp. 492-508 | DOI

[40] Shimodaira, H.; Hasegawa, M. Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference, Molecular Biology and Evolution, Volume 16 (1999) no. 8, pp. 1114-1116 | DOI

[41] Strimmer, K.; Rambaut, A. Inferring confidence sets of possibly misspecified gene trees, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 269 (2002) no. 1487, pp. 137-142 | DOI

[42] Wingstrand, K. Comparative spermatology of the Crustacea Entomostraca; 1, Subclass Branchiopoda, Biologiske Skrifter, Volume 22 (1978)

[43] Wuerz, M.; Huebner, E.; Huebner, J. The morphology of the male reproductive system, spermatogenesis and the spermatozoon of<i>Daphnia magna</i>(Crustacea: Branchiopoda), Journal of Morphology, Volume 278 (2017) no. 11, pp. 1536-1550 | DOI

[44] Xu, S.; Ackerman, M. S.; Long, H.; Bright, L.; Spitze, K.; Ramsdell, J. S.; Thomas, W. K.; Lynch, M. A Male-Specific Genetic Map of the Microcrustacean <i>Daphnia pulex</i> Based on Single-Sperm Whole-Genome Sequencing, Genetics, Volume 201 (2015) no. 1, pp. 31-38 | DOI

[45] Zaffagnini, F. Reproduction in Daphnia In: Daphnia (R. H. Peters & R. De Bernadi , eds), Istituto Italiano di Idrobiologia, Pallanza, Italy (1987)

Cited by Sources: