Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology

Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process?

10.24072/pcjournal.135 - Peer Community Journal, Volume 2 (2022), article no. e37.

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Hymenopterans are haplodiploids and unlike most other Arthropods they do not possess sexual chromosomes. Sex determination typically happens via the ploidy of individuals: haploids become males and diploids become females. Arrhenotoky is believed to be the ancestral reproduction mode in Hymenopterans, with haploid males produced parthenogenetically, and diploid females produced sexually. However, a number of transitions towards thelytoky (diploid females produced parthenogenetically) have appeared in Hymenopterans, and in most cases populations or species are either totally arrhenotokous or totally thelytokous. Here we present the case of Cotesia typhae (Fernandez-Triana), a Braconidae that produces parthenogenetic females at a low frequency. The phenotyping of two laboratory strains and one natural population showed that this frequency is variable, and that this rare thelytokous phenomenon also happens in the wild. Moreover, mated females from one of the laboratory strains produce a few parthenogenetic daughters among a majority of sexual daughters. The analysis of daughters of heterozygous virgin females allowed us to show that a mechanism similar to automixis with central fusion is very likely at play in C. typhae. This mechanism allows some parts of the genome to remain heterozygous, especially at the chromosomes’ centromeres, which can be advantageous depending on the sex determination system involved. Lastly, in most species, the origin of thelytoky is either bacterial or genetic, and an antibiotic treatment as well as PCR experiments did not demonstrate a bacterial cause in C. typhae. The unusual case of low parthenogenetic frequency described in this species constitutes another example of the fascinating diversity of sex determination systems in Arthropods.

Published online:
DOI: 10.24072/pcjournal.135
Type: Research article

Capdevielle Dulac, Claire 1; Benoist, Romain 1; Paquet, Sarah 1; Calatayud, Paul-André 1; Obonyo, Julius 2; Kaiser, Laure 1; Mougel, Florence 1

1 Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie – 91198, Gif-sur-Yvette, France
2 icipe, International Center of Insect Physiology and Ecology, P.O. Box 30772-00100 – Nairobi, Kenya
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Capdevielle Dulac, Claire and Benoist, Romain and Paquet, Sarah and Calatayud, Paul-Andr\'e and Obonyo, Julius and Kaiser, Laure and Mougel, Florence},
     title = {Spontaneous parthenogenesis in the parasitoid wasp {\protect\emph{Cotesia} typhae}: low frequency anomaly or evolving process?},
     journal = {Peer Community Journal},
     eid = {e37},
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     year = {2022},
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%A Paquet, Sarah
%A Calatayud, Paul-André
%A Obonyo, Julius
%A Kaiser, Laure
%A Mougel, Florence
%T Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process?
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Capdevielle Dulac, Claire; Benoist, Romain; Paquet, Sarah; Calatayud, Paul-André; Obonyo, Julius; Kaiser, Laure; Mougel, Florence. Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process?. Peer Community Journal, Volume 2 (2022), article  no. e37. doi : 10.24072/pcjournal.135.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100141

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] Aamidor, S. E.; Yagound, B.; Ronai, I.; Oldroyd, B. P. Sex mosaics in the honeybee: how haplodiploidy makes possible the evolution of novel forms of reproduction in social Hymenoptera, Biology Letters, Volume 14 (2018) no. 11 | DOI

[2] Adachi-Hagimori, T.; Miura, K.; Stouthamer, R. A new cytogenetic mechanism for bacterial endosymbiont-induced parthenogenesis in Hymenoptera, Proceedings of the Royal Society B: Biological Sciences, Volume 275 (2008) no. 1652, pp. 2667-2673 | DOI

[3] Archetti, M. Evidence from automixis with inverted meiosis for the maintenance of sex by loss of complementation, Journal of Evolutionary Biology, Volume 35 (2022) no. 1, pp. 40-50 | DOI

[4] Archetti, M. Complementation, Genetic Conflict, and the Evolution of Sex and Recombination, Journal of Heredity, Volume 101 (2010) no. Supplement 1 | DOI

[5] Ball, S. L. Tychoparthenogenesis and mixed mating in natural populations of the mayfly Stenonema femoratum, Heredity, Volume 87 (2001) no. 3, pp. 373-380 | DOI

[6] Baudry, E.; Kryger, P.; Allsopp, M.; Koeniger, N.; Vautrin, D.; Mougel, F.; Cornuet, J.-M.; Solignac, M. Whole-Genome Scan in Thelytokous-Laying Workers of the Cape Honeybee (Apis mellifera capensis): Central Fusion, Reduced Recombination Rates and Centromere Mapping Using Half-Tetrad Analysis, Genetics, Volume 167 (2004) no. 1, pp. 243-252 | DOI

[7] Benoist, R.; Capdevielle‐Dulac, C.; Chantre, C.; Jeannette, R.; Calatayud, P.; Drezen, J.; Dupas, S.; Le Rouzic, A.; Le Ru, B.; Moreau, L.; Van Dijk, E.; Kaiser, L.; Mougel, F. Quantitative trait loci involved in the reproductive success of a parasitoid wasp, Molecular Ecology, Volume 29 (2020) no. 18, pp. 3476-3493 | DOI

[8] Benoist, R.; Chantre, C.; Capdevielle-Dulac, C.; Bodet, M.; Mougel, F.; Calatayud, P. A.; Dupas, S.; Huguet, E.; Jeannette, R.; Obonyo, J.; Odorico, C.; Silvain, J. F.; Le Ru, B.; Kaiser, L. Relationship between oviposition, virulence gene expression and parasitism success in Cotesia typhae nov. sp. parasitoid strains, Genetica, Volume 145 (2017) no. 6, pp. 469-479 | DOI

[9] Benoist, R.; Paquet, S.; Decourcelle, F.; Guez, J.; Jeannette, R.; Calatayud, P.-A.; Le Ru, B.; Mougel, F.; Kaiser, L. Role of egg-laying behavior, virulence and local adaptation in a parasitoid’s chances of reproducing in a new host, Journal of Insect Physiology, Volume 120 (2020) | DOI

[10] Beukeboom, L. W.; Pijnacker, L. P. Automictic parthenogenesis in the parasitoid<i>Venturia canescens</i>(Hymenoptera: Ichneumonidae) revisited, Genome, Volume 43 (2000) no. 6, pp. 939-944 | DOI

[11] Boivin, G. Sperm as a limiting factor in mating success in Hymenoptera parasitoids, Entomologia Experimentalis et Applicata, Volume 146 (2013) no. 1, pp. 149-155 | DOI

[12] Bourge, M.; Brown, S. C.; Siljak-Yakovlev, S. Flow cytometry as tool in plant sciences, with emphasis on genome size and ploidy level assessment, Genetics &amp; Applications, Volume 2 (2018) no. 2, pp. 1-12 | DOI

[13] Branca, A.; Le Ru, B.; Calatayud, P.-A.; Obonyo, J.; Musyoka, B.; Capdevielle-Dulac, C.; Kaiser-Arnauld, L.; Silvain, J.-F.; Gauthier, J.; Paillusson, C.; Gayral, P.; Herniou, E. A.; Dupas, S. Relative Influence of Host, Wolbachia, Geography and Climate on the Genetic Structure of the Sub-saharan Parasitic Wasp Cotesia sesamiae, Frontiers in Ecology and Evolution, Volume 7 (2019) | DOI

[14] Casiraghi, M.; Bordenstein, S. R.; Baldo, L.; Lo, N.; Beninati, T.; Wernegreen, J. J.; Werren, J. H.; Bandi, C. Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree, Microbiology, Volume 151 (2005) no. 12, pp. 4015-4022 | DOI

[15] Chapman, N. C.; Beekman, M.; Allsopp, M. H.; Rinderer, T. E.; Lim, J.; Oxley, P. R.; Oldroyd, B. P. Inheritance of thelytoky in the honey bee Apis mellifera capensis, Heredity, Volume 114 (2015) no. 6, pp. 584-592 | DOI

[16] Collet, M.; Amat, I.; Sauzet, S.; Auguste, A.; Fauvergue, X.; Mouton, L.; Desouhant, E. Insects and incest: Sib‐mating tolerance in natural populations of a parasitoid wasp, Molecular Ecology, Volume 29 (2020) no. 3, pp. 596-609 | DOI

[17] de Boer, J. G.; Groenen, M. A.; Pannebakker, B. A.; Beukeboom, L. W.; Kraus, R. H. Population-level consequences of complementary sex determination in a solitary parasitoid, BMC Evolutionary Biology, Volume 15 (2015) no. 1 | DOI

[18] de Boer, J. G.; Kuijper, B.; Heimpel, G. E.; Beukeboom, L. W. Sex determination meltdown upon biological control introduction of the parasitoid<i>Cotesia rubecula?</i>, Evolutionary Applications, Volume 5 (2012) no. 5, pp. 444-454 | DOI

[19] Dwight, Z. L.; Palais, R.; Wittwer, C. T. uAnalyze: Web-Based High-Resolution DNA Melting Analysis with Comparison to Thermodynamic Predictions, IEEE/ACM Transactions on Computational Biology and Bioinformatics, Volume 9 (2012) no. 6, pp. 1805-1811 | DOI

[20] Ferree, P. M.; Aldrich, J. C.; Jing, X. A.; Norwood, C. T.; Van Schaick, M. R.; Cheema, M. S.; Ausió, J.; Gowen, B. E. Spermatogenesis in haploid males of the jewel wasp Nasonia vitripennis, Scientific Reports, Volume 9 (2019) no. 1 | DOI

[21] Foray, V.; Henri, H.; Martinez, S.; Gibert, P.; Desouhant, E. Occurrence of arrhenotoky and thelytoky in a parasitic wasp Venturia canescens (Hymenoptera: Ichneumonidae): Effect of endosymbionts or existence of two distinct reproductive modes?, European Journal of Entomology, Volume 110 (2013) no. 1, pp. 103-107 | DOI

[22] Giorgini, M.; Monti, M. M.; Caprio, E.; Stouthamer, R.; Hunter, M. S. Feminization and the collapse of haplodiploidy in an asexual parasitoid wasp harboring the bacterial symbiont Cardinium, Heredity, Volume 102 (2009) no. 4, pp. 365-371 | DOI

[23] Gloag, R.; Remnant, E. J.; Oldroyd, B. P. The frequency of thelytokous parthenogenesis in European-derived Apis mellifera virgin queens, Apidologie, Volume 50 (2019) no. 3, pp. 295-303 | DOI

[24] Gokhman, V. E.; Kuznetsova, V. G. Parthenogenesis in Hexapoda: holometabolous insects, Journal of Zoological Systematics and Evolutionary Research, Volume 56 (2017) no. 1, pp. 23-34 | DOI

[25] Gu, H.; Dorn, S. Mating system and sex allocation in the gregarious parasitoid Cotesia glomerata, Animal Behaviour, Volume 66 (2003) no. 2, pp. 259-264 | DOI

[26] Hedrick, P. W.; Parker, J. D. Evolutionary Genetics and Genetic Variation of Haplodiploids and X-Linked Genes, Annual Review of Ecology and Systematics, Volume 28 (1997) no. 1, pp. 55-83 | DOI

[27] Heimpel, G. E.; de Boer, J. G. Sex Determination in the Hymenoptera, Annual Review of Entomology, Volume 53 (2008) no. 1, pp. 209-230 | DOI

[28] Henter, H. J. Inbreeding depression and haplodiploidy: experimental measures in a parasitoid and comparisons across diploid and haplodiploid insect taxa, Evolution, Volume 57 (2003) no. 8, pp. 1793-1803 | DOI

[29] Jarosch, A.; Stolle, E.; Crewe, R. M.; Moritz, R. F. A. Alternative splicing of a single transcription factor drives selfish reproductive behavior in honeybee workers ( <i>Apis mellifera</i> ), Proceedings of the National Academy of Sciences, Volume 108 (2011) no. 37, pp. 15282-15287 | DOI

[30] Kaiser, L.; Fernandez-Triana, J.; Capdevielle-Dulac, C.; Chantre, C.; Bodet, M.; Kaoula, F.; Benoist, R.; Calatayud, P.-A.; Dupas, S.; Herniou, E. A.; Jeannette, R.; Obonyo, J.; Silvain, J.-F.; Le Ru, B. Systematics and biology of Cotesia typhae sp. n. (Hymenoptera, Braconidae, Microgastrinae), a potential biological control agent against the noctuid Mediterranean corn borer, Sesamia nonagrioides, ZooKeys, Volume 682 (2017), pp. 105-136 | DOI

[31] Kaiser, L.; Le Ru, B. P.; Kaoula, F.; Paillusson, C.; Capdevielle‐Dulac, C.; Obonyo, J. O.; Herniou, E. A.; Jancek, S.; Branca, A.; Calatayud, P.; Silvain, J.; Dupas, S. Ongoing ecological speciation in <i>Cotesia sesamiae</i> , a biological control agent of cereal stem borers, Evolutionary Applications, Volume 8 (2015) no. 8, pp. 807-820 | DOI

[32] Lattorff, H. M. G.; Moritz, R. F. A.; Fuchs, S. A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis), Heredity, Volume 94 (2005) no. 5, pp. 533-537 | DOI

[33] Leach, I. M.; Pannebakker, B. A.; Schneider, M. V.; Driessen, G.; van de Zande, L.; Beukeboom, L. W. Thelytoky in Hymenoptera with Venturia canescens and Leptopilina clavipes as Case Studies, Lost Sex, Springer Netherlands, Dordrecht, 2009, pp. 347-375 | DOI

[34] Liegeois, M.; Sartori, M.; Schwander, T. Extremely Widespread Parthenogenesis and a Trade-Off Between Alternative Forms of Reproduction in Mayflies (Ephemeroptera), Journal of Heredity, Volume 112 (2021) no. 1, pp. 45-57 | DOI

[35] Little, C. J.; Chapuis, M.-P.; Blondin, L.; Chapuis, E.; Jourdan-Pineau, H. Exploring the relationship between tychoparthenogenesis and inbreeding depression in the Desert Locust, <i>Schistocerca gregaria</i>, Ecology and Evolution, Volume 7 (2017) no. 15, pp. 6003-6011 | DOI

[36] Liu, Q.-q.; Zhou, J.-c.; Zhang, C.; Ning, S.-f.; Duan, L.-j.; Dong, H. Co-occurrence of thelytokous and bisexual Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae) in a natural population, Scientific Reports, Volume 9 (2019) no. 1 | DOI

[37] Ma, W.-J.; Schwander, T. Patterns and mechanisms in instances of endosymbiont-induced parthenogenesis, Journal of Evolutionary Biology, Volume 30 (2017) no. 5, pp. 868-888 | DOI

[38] Mackensen, O. The Occurrence of Parthenogenetic Females in Some Strains of Honeybees, Journal of Economic Entomology, Volume 36 (1943) no. 3, pp. 465-467 | DOI

[39] Meirmans, S.; Meirmans, P. G.; Kirkendall, L. R. The Costs Of Sex: Facing Real-world Complexities, The Quarterly Review of Biology, Volume 87 (2012) no. 1, pp. 19-40 | DOI

[40] Mochiah, M. B.; Ngi-Song, A. J.; Overholt, W. A.; Stouthamer, R. Wolbachia infection in Cotesia sesamiae (Hymenoptera: Braconidae) causes cytoplasmic incompatibility: implications for biological control, Biological Control, Volume 25 (2002) no. 1, pp. 74-80 | DOI

[41] Morgan-Richards, M.; Trewick, S. A. Hybrid origin of a parthenogenetic genus?, Molecular Ecology, Volume 14 (2005) no. 7, pp. 2133-2142 | DOI

[42] Neiman, M.; Sharbel, T. F.; Schwander, T. Genetic causes of transitions from sexual reproduction to asexuality in plants and animals, Journal of Evolutionary Biology, Volume 27 (2014) no. 7, pp. 1346-1359 | DOI

[43] Neumann, P. Social parasitism by honeybee workers (Apis mellifera capensis Escholtz): host finding and resistance of hybrid host colonies, Behavioral Ecology, Volume 12 (2001) no. 4, pp. 419-428 | DOI

[44] Otto, S. P. The Evolutionary Enigma of Sex, The American Naturalist, Volume 174 (2009) no. S1 | DOI

[45] Pardo, M. C.; López-León, M. D.; Cabrero, J.; Camacho, J. P. M. Cytological and developmental analysis of tychoparthenogenesis in Locusta migratoria, Heredity, Volume 75 (1995) no. 5, pp. 485-494 | DOI

[46] Pijls, J. W. A. M.; van Steenbergen, H. J.; van Alphen, J. J. M. Asexuality cured: the relations and differences between sexual and asexual Apoanagyrus diversicornis, Heredity, Volume 76 (1996) no. 5, pp. 506-513 | DOI

[47] Rabeling, C.; Kronauer, D. J. Thelytokous Parthenogenesis in Eusocial Hymenoptera, Annual Review of Entomology, Volume 58 (2013) no. 1, pp. 273-292 | DOI

[48] Rey, O.; Loiseau, A.; Facon, B.; Foucaud, J.; Orivel, J.; Cornuet, J.-M.; Robert, S.; Dobigny, G.; Delabie, J. H. C.; Mariano, C. D. S. F.; Estoup, A. Meiotic Recombination Dramatically Decreased in Thelytokous Queens of the Little Fire Ant and Their Sexually Produced Workers, Molecular Biology and Evolution, Volume 28 (2011) no. 9, pp. 2591-2601 | DOI

[49] Sandrock, C.; Vorburger, C. Single-Locus Recessive Inheritance of Asexual Reproduction in a Parasitoid Wasp, Current Biology, Volume 21 (2011) no. 5, pp. 433-437 | DOI

[50] Schneider, M. V.; Beukeboom, L. W.; Driessen, G.; Lapchin, L.; Bernstein, C.; Van Alphen, J. J. M. Geographical distribution and genetic relatedness of sympatrical thelytokous and arrhenotokous populations of the parasitoid Venturia canescens (Hymenoptera), Journal of Evolutionary Biology, Volume 15 (2002) no. 2, pp. 191-200 | DOI

[51] Song, Y.; Scheu, S.; Drossel, B. The ecological advantage of sexual reproduction in multicellular long-lived organisms, Journal of Evolutionary Biology, Volume 25 (2012) no. 3, pp. 556-565 | DOI

[52] Stouthamer, R.; Pinto, J. D.; Platner, G. R.; Luck, R. F. Taxonomic Status of Thelytokous Forms of Trichogramma (Hymenoptera: Trichogrammatidae), Annals of the Entomological Society of America, Volume 83 (1990) no. 3, pp. 475-481 | DOI

[53] Tree of Sex: A database of sexual systems, Scientific Data, Volume 1 (2014) no. 1 | DOI

[54] Tsutsui, Y.; Maeto, K.; Hamaguchi, K.; Isaki, Y.; Takami, Y.; Naito, T.; Miura, K. Apomictic parthenogenesis in a parasitoid wasp<i>Meteorus pulchricornis</i>, uncommon in the haplodiploid order Hymenoptera, Bulletin of Entomological Research, Volume 104 (2014) no. 3, pp. 307-313 | DOI

[55] Tucker, K. W. Automictic parthenogenesis in the honey bee, Genetics, Volume 43 (1958) no. 3, pp. 299-316 | DOI

[56] Tvedte, E. S.; Logsdon, J. M.; Forbes, A. A. Sex loss in insects: causes of asexuality and consequences for genomes, Current Opinion in Insect Science, Volume 31 (2019), pp. 77-83 | DOI

[57] van de Zande, L.; Verhulst, E. Genomic Imprinting and Maternal Effect Genes in Haplodiploid Sex Determination, Sexual Development, Volume 8 (2014) no. 1-3, pp. 74-82 | DOI

[58] van der Kooi, C. J.; Matthey-Doret, C.; Schwander, T. Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods, Evolution Letters, Volume 1 (2017) no. 6, pp. 304-316 | DOI

[59] van Wilgenburg, E.; Driessen, G.; Beukeboom, L. W. Single locus complementary sex determination in Hymenoptera: an "unintelligent" design?, Frontiers in Zoology, Volume 3 (2006) no. 1 | DOI

[60] van der Kooi, C. J.; Schwander, T. Parthenogenesis: Birth of a New Lineage or Reproductive Accident?, Current Biology, Volume 25 (2015) no. 15 | DOI

[61] Verma, S.; Ruttner, F. Cytological analysis of the thelytokous parthenogenesis in the cape honeybee (Apis mellifera capensis escholtz), Apidologie, Volume 14 (1983) no. 1, pp. 41-57 | DOI

[62] Vershinina, A. O.; Kuznetsova, V. G. Parthenogenesis in Hexapoda: Entognatha and non-holometabolous insects, Journal of Zoological Systematics and Evolutionary Research, Volume 54 (2016) no. 4, pp. 257-268 | DOI

[63] Vorburger, C. Thelytoky and Sex Determination in the Hymenoptera: Mutual Constraints, Sexual Development, Volume 8 (2014) no. 1-3, pp. 50-58 | DOI

[64] Weeks, E. N.; Birkett, M. A.; Cameron, M. M.; Pickett, J. A.; Logan, J. G. Semiochemicals of the common bed bug, <i>Cimex lectularius</i> L. (Hemiptera: Cimicidae), and their potential for use in monitoring and control, Pest Management Science, Volume 67 (2010) no. 1, pp. 10-20 | DOI

[65] Whiting, P. W. The Evolution of Male Haploidy, The Quarterly Review of Biology, Volume 20 (1945) no. 3, pp. 231-260 | DOI

[66] Zchori-Fein, E.; Perlman, S. J. Distribution of the bacterial symbiont Cardinium in arthropods, Molecular Ecology, Volume 13 (2004) no. 7, pp. 2009-2016 | DOI

[67] Zhou, Y.; Gu, H.; Dorn, S. Effects of inbreeding on fitness components of Cotesia glomerata, a parasitoid wasp with single-locus complementary sex determination (sl-CSD), Biological Control, Volume 40 (2007) no. 2, pp. 273-279 | DOI

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