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

Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?

Larose, Chloé1  ; Lavanchy, Guillaume1   ; Freitas, Susana1 ; Parker, Darren J.2, 3 ; Schwander, Tanja1 
1 Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland
2 Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne
3 School of Natural Sciences, Brambell Building, Bangor University, Bangor, LL57 2UW, United Kingdom

Corresponding author(s): Lavanchy, Guillaume (guillaume.lavanchy@unil.ch)

10.24072/pcjournal.283 - Peer Community Journal, Volume 3 (2023), article no. e60.

Get full text PDF Peer reviewed and recommended by PCI
article image

Transitions from obligate sex to obligate parthenogenesis have occurred repeatedly across the tree of life. Whether these transitions occur abruptly or via a transient phase of facultative parthenogenesis is rarely known. We discovered and characterised facultatively parthenogenetic populations of the North American stick insect Timema douglasi, a species in which only obligately parthenogenetic populations were known so far. These populations comprised three genetic lineages. Females from all lineages were capable of parthenogenesis (with variable efficiency) but their propensity to reproduce sexually after mating varied extensively. In all three lineages, parthenogenesis resulted in the complete loss of heterozygosity in a single generation. Obligately parthenogenetic Timema have also lost all heterozygosity, suggesting that the transition to obligate parthenogenesis did not require a modification of the proximate mechanism, but rather involved a gradual increase in frequency. We speculate that facultative parthenogenesis may often be transient and be replaced by obligate strategies (either sex or parthenogenesis) because of a trade-off between the efficiency of the two reproductive modes. Such a trade-off could help explain why facultative parthenogenesis is rare among animals, despite its potential to combine the known benefits of sex and parthenogenesis.

Published online:
DOI: 10.24072/pcjournal.283
Type: Research article
Keywords: Timema douglasi, Phasmatodea, gamete duplication, automixis, heterozygosity, RAD sequencing, reproductive system, reproductive mode.

Larose, Chloé 1; Lavanchy, Guillaume 1; Freitas, Susana 1; Parker, Darren J. 2, 3; Schwander, Tanja 1

1 Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne, Switzerland
2 Department of Ecology and Evolution, University of Lausanne, 1015 Lausanne
3 School of Natural Sciences, Brambell Building, Bangor University, Bangor, LL57 2UW, United Kingdom
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_283,
     author = {Larose, Chlo\'e and Lavanchy, Guillaume and Freitas, Susana and Parker, Darren J. and Schwander, Tanja},
     title = {Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?},
     journal = {Peer Community Journal},
     eid = {e60},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.283},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.283/}
}
TY  - JOUR
AU  - Larose, Chloé
AU  - Lavanchy, Guillaume
AU  - Freitas, Susana
AU  - Parker, Darren J.
AU  - Schwander, Tanja
TI  - Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.283/
DO  - 10.24072/pcjournal.283
LA  - en
ID  - 10_24072_pcjournal_283
ER  - 
%0 Journal Article
%A Larose, Chloé
%A Lavanchy, Guillaume
%A Freitas, Susana
%A Parker, Darren J.
%A Schwander, Tanja
%T Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.283/
%R 10.24072/pcjournal.283
%G en
%F 10_24072_pcjournal_283
Larose, Chloé; Lavanchy, Guillaume; Freitas, Susana; Parker, Darren J.; Schwander, Tanja. Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?. Peer Community Journal, Volume 3 (2023), article  no. e60. doi : 10.24072/pcjournal.283. https://peercommunityjournal.org/articles/10.24072/pcjournal.283/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100551

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] Arbuthnott, D.; Crespi, B. J.; Schwander, T. Female Stick Insects Mate Multiply to Find Compatible Mates, The American Naturalist, Volume 186 (2015) no. 4, pp. 519-530 | DOI

[2] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using lme4, Journal of Statistical Software, Volume 67 (2015) no. 1 | DOI

[3] Bell, G. The Masterpiece of Nature: The Evolution and Genetics of Sexuality., University of California Press, 1982

[4] Bolger, A. M.; Lohse, M.; Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, Volume 30 (2014) no. 15, pp. 2114-2120 | DOI

[5] Booth, W.; Smith, C. F.; Eskridge, P. H.; Hoss, S. K.; Mendelson, J. R.; Schuett, G. W. Facultative parthenogenesis discovered in wild vertebrates, Biology Letters, Volume 8 (2012) no. 6, pp. 983-985 | DOI

[6] Boyer, L.; Jabbour-Zahab, R.; Mosna, M.; Haag, C. R.; Lenormand, T. Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica, Evolution Letters, Volume 5 (2021) no. 2, pp. 164-174 | DOI

[7] Brelsford, A.; Dufresnes, C.; Perrin, N. High-density sex-specific linkage maps of a European tree frog (Hyla arborea) identify the sex chromosome without information on offspring sex, Heredity, Volume 116 (2015) no. 2, pp. 177-181 | DOI

[8] Brown, T. A.; Tsurusaki, N.; Burns, M. Genomic Determination of Reproductive Mode in Facultatively Parthenogenetic Opiliones, Journal of Heredity, Volume 112 (2021) no. 1, pp. 34-44 | DOI

[9] Burke, N. W.; Bonduriansky, R. Sexual Conflict, Facultative Asexuality, and the True Paradox of Sex, Trends in Ecology & Evolution, Volume 32 (2017) no. 9, pp. 646-652 | DOI

[10] Burke, N. W.; Bonduriansky, R. The geography of sex: sexual conflict, environmental gradients and local loss of sex in facultatively parthenogenetic animals, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 373 (2018) no. 1757 | DOI

[11] Catchen, J.; Hohenlohe, P. A.; Bassham, S.; Amores, A.; Cresko, W. A. Stacks: an analysis tool set for population genomics, Molecular Ecology, Volume 22 (2013) no. 11, pp. 3124-3140 | DOI

[12] Cuellar, O. On the Origin of Parthenogenesis in Vertebrates: The Cytogenetic Factors, The American Naturalist, Volume 108 (1974) no. 963, pp. 625-648 | DOI

[13] Danecek, P.; Auton, A.; Abecasis, G.; Albers, C. A.; Banks, E.; DePristo, M. A.; Handsaker, R. E.; Lunter, G.; Marth, G. T.; Sherry, S. T.; McVean, G.; Durbin, R. The variant call format and VCFtools, Bioinformatics, Volume 27 (2011) no. 15, pp. 2156-2158 | DOI

[14] de Vichet, G. Découverte dans le sud de la France d’une station de males de Bacillus rossii (Fabr.) (Orthoptère, Phasmidae), Publications de la Société Linnéenne de Lyon, Volume 13 (1944) no. 6, pp. 92-94

[15] Delmotte, F.; Leterme, N.; Bonhomme, J.; Rispe, C.; Simon, J.-C. Multiple routes to asexuality in an aphid species, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 268 (2001) no. 1483, pp. 2291-2299 | DOI

[16] D'Souza, T. G.; Michiels, N. K. The Costs and Benefits of Occasional Sex: Theoretical Predictions and a Case Study, Journal of Heredity, Volume 101 (2010) no. Supplement 1, p. S34-S41 | DOI

[17] 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

[18] Fields, A. T.; Feldheim, K. A.; Poulakis, G. R.; Chapman, D. D. Facultative parthenogenesis in a critically endangered wild vertebrate, Current Biology, Volume 25 (2015) no. 11 | DOI

[19] Fox, J.; Weisberg, S. An R Companion to Applied Regression (Third edition), Sage, 2019

[20] Freitas, S.; Parker, D. J.; Labédan, M.; Dumas, Z.; Schwander, T. Evidence for cryptic gene flow in parthenogenetic stick insects of the genus Timema, BioRxiv, 2023 | DOI

[21] Lavanchy, G.; Parker, D. J. glavanc1/Timema_facultative_partheno: Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects? (tag), Zenodo, 2023 | DOI

[22] Groot, T. V. M.; Bruins, E.; Breeuwer, J. A. J. Molecular genetic evidence for parthenogenesis in the Burmese python, Python molurus bivittatus, Heredity, Volume 90 (2003) no. 2, pp. 130-135 | DOI

[23] Helleu, Q.; Gérard, P. R.; Montchamp-Moreau, C. Sex Chromosome Drive, Cold Spring Harbor Perspectives in Biology, Volume 7 (2014) no. 2 | DOI

[24] Hothorn, T.; Bretz, F.; Westfall, P. Simultaneous Inference in General Parametric Models, Biometrical Journal, Volume 50 (2008) no. 3, pp. 346-363 | DOI

[25] Innes, D. J.; Hebert, P. D. N. The Origin and Genetic Basis of Obligate Parthenogenesis in Daphnia pulex, Evolution, Volume 42 (1988) no. 5, pp. 1024-1035 | DOI

[26] Jaegle, B.; Pisupati, R.; Soto-Jiménez, L. M.; Burns, R.; Rabanal, F. A.; Nordborg, M. Extensive gene duplication in Arabidopsis revealed by pseudo-heterozygosity, bioRxiv, 2021 | DOI

[27] Jaenike, J. Sex Chromosome Meiotic Drive, Annual Review of Ecology and Systematics, Volume 32 (2001) no. 1, pp. 25-49 | DOI

[28] Jaron, K. S.; Parker, D. J.; Anselmetti, Y.; Tran Van, P.; Bast, J.; Dumas, Z.; Figuet, E.; François, C. M.; Hayward, K.; Rossier, V.; Simion, P.; Robinson-Rechavi, M.; Galtier, N.; Schwander, T. Convergent consequences of parthenogenesis on stick insect genomes, Science Advances, Volume 8 (2022) no. 8 | DOI

[29] Knaus, B. J.; Grünwald, N. J. vcfr: a package to manipulate and visualize variant call format data in R, Molecular Ecology Resources, Volume 17 (2016) no. 1, pp. 44-53 | DOI

[30] Kratochvíl, L.; Vukić, J.; Červenka, J.; Kubička, L.; Johnson Pokorná, M.; Kukačková, D.; Rovatsos, M.; Piálek, L. Mixed‐sex offspring produced via cryptic parthenogenesis in a lizard, Molecular Ecology, Volume 29 (2020) no. 21, pp. 4118-4127 | DOI

[31] Kuhn, A.; Aron, S.; Hardy, O. J. Detection of Cryptic Sex in Automictic Populations: Theoretical Expectations and a Case Study in Cataglyphis Desert Ants, Frontiers in Ecology and Evolution, Volume 9 (2021) | DOI

[32] Laine, V. N.; Sackton, T. B.; Meselson, M. Genomic signature of sexual reproduction in the bdelloid rotifer Macrotrachella quadricornifera, Genetics, Volume 220 (2021) no. 2 | DOI

[33] Li, H.; Durbin, R. Fast and accurate long-read alignment with Burrows–Wheeler transform, Bioinformatics, Volume 26 (2010) no. 5, pp. 589-595 | 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 (2020) no. 1, pp. 45-57 | DOI

[35] 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

[36] Morgan‐Richards, M.; Langton‐Myers, S. S.; Trewick, S. A. Loss and gain of sexual reproduction in the same stick insect, Molecular Ecology, Volume 28 (2019) no. 17, pp. 3929-3941 | DOI

[37] 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

[38] Normark, B. B. The evolution of alternative genetic systems in insects, Annual Review of Entomology, Volume 48 (2003) no. 1, pp. 397-423 | DOI

[39] Otto, S. P. The Evolutionary Enigma of Sex, The American Naturalist, Volume 174 (2009) no. S1, p. S1-S14 | DOI

[40] Pearcy, M.; Hardy, O.; Aron, S. Thelytokous parthenogenesis and its consequences on inbreeding in an ant, Heredity, Volume 96 (2006) no. 5, pp. 377-382 | DOI

[41] Pijnacker, L. P.; Ferwerda, M. A. Sex chromosomes and origin of males and sex mosaics of the parthenogenetic stick insect Carausius morosus Br., Chromosoma, Volume 79 (1980) no. 1, pp. 105-114 | DOI

[42] Quinlan, A. R.; Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features, Bioinformatics, Volume 26 (2010) no. 6, pp. 841-842 | DOI

[43] R Core Team R: A language and environment for statistical computing, R Foundation for Statistical Computing, 2021

[44] Raj, A.; Stephens, M.; Pritchard, J. K. fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets, Genetics, Volume 197 (2014) no. 2, pp. 573-589 | DOI

[45] Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things), Methods in Ecology and Evolution, Volume 3 (2011) no. 2, pp. 217-223 | DOI

[46] Ryder, O. A.; Thomas, S.; Judson, J. M.; Romanov, M. N.; Dandekar, S.; Papp, J. C.; Sidak-Loftis, L. C.; Walker, K.; Stalis, I. H.; Mace, M.; Steiner, C. C.; Chemnick, L. G. Corrigendum to: Facultative Parthenogenesis in California Condors, Journal of Heredity, Volume 113 (2021) no. 2, p. 217-217 | DOI

[47] Sandoval, C. Persistence of a Walking-Stick Population (Phasmatoptera: Timematodea) after a Wildfire, The Southwestern Naturalist, Volume 45 (2000) no. 2 | DOI

[48] Sandoval, C.; Carmean, D.; Crespi, B. Molecular phylogenetics of sexual and parthenogenetic Timema walking–sticks, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 265 (1998) no. 1396, pp. 589-595 | 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] Schultz, R. J. Unisexual Fish: Laboratory Synthesis of a "Species", Science, Volume 179 (1973) no. 4069, pp. 180-181 | DOI

[51] Schurko, A. M.; Neiman, M.; Logsdon, J. M. Signs of sex: what we know and how we know it, Trends in Ecology & Evolution, Volume 24 (2009) no. 4, pp. 208-217 | DOI

[52] Schwander, T.; Crespi, B. J. Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects, Evolution, Volume 63 (2009) no. 1, pp. 84-103 | DOI

[53] Schwander, T.; Crespi, B. J.; Gries, R.; Gries, G. Neutral and selection-driven decay of sexual traits in asexual stick insects, Proceedings of the Royal Society B: Biological Sciences, Volume 280 (2013) no. 1764 | DOI

[54] Schwander, T.; Henry, L.; Crespi, B. J. Molecular Evidence for Ancient Asexuality in Timema Stick Insects, Current Biology, Volume 21 (2011) no. 13, pp. 1129-1134 | DOI

[55] Schwander, T.; Vuilleumier, S.; Dubman, J.; Crespi, B. J. Positive feedback in the transition from sexual reproduction to parthenogenesis, Proceedings of the Royal Society B: Biological Sciences, Volume 277 (2010) no. 1686, pp. 1435-1442 | DOI

[56] Simon, C.; Frati, F.; Beckenbach, A.; Crespi, B.; Liu, H.; Flook, P. Evolution, Weighting, and Phylogenetic Utility of Mitochondrial Gene Sequences and a Compilation of Conserved Polymerase Chain Reaction Primers, Annals of the Entomological Society of America, Volume 87 (1994) no. 6, pp. 651-701 | DOI

[57] Moritz, C.; Suomalainen, E.; Saura, A.; Lokki, J. Cytology and Evolution in Parthenogenesis, Evolution, Volume 44 (1990) no. 4 | DOI

[58] Svendsen, N.; Reisser, C. M. O.; Dukić, M.; Thuillier, V.; Ségard, A.; Liautard-Haag, C.; Fasel, D.; Hürlimann, E.; Lenormand, T.; Galimov, Y.; Haag, C. R. Uncovering Cryptic Asexuality in Daphnia magna by RAD Sequencing, Genetics, Volume 201 (2015) no. 3, pp. 1143-1155 | DOI

[59] Ashman, T.-L.; Bachtrog, D.; Blackmon, H.; Goldberg, E. E.; Hahn, M. W.; Kirkpatrick, M.; Kitano, J.; Mank, J. E.; Mayrose, I.; Ming, R.; Otto, S. P.; Peichel, C. L.; Pennell, M. W.; Perrin, N.; Ross, L.; Valenzuela, N.; Vamosi, J. C. Tree of Sex: A database of sexual systems, Scientific Data, Volume 1 (2014) no. 1 | DOI

[60] Vickery, V. R.; Sandoval, C. P. Two new species of Timema (Phasmatoptera: Timematodea: Timematidae), one parthenogenetic, in California, Journal of Orthoptera Research, Volume 10 (2001) no. 1, pp. 53-61

[61] Vickery, V. R.; Sandoval, C. P. Descriptions of three new species of Timema (Phasmatoptera: Timematodea: Timematidae) and notes on three other species, Journal of Orthoptera Research, Volume 10 (2001) no. 1, pp. 53-61 | DOI

Cited by Sources:

block.super