Paternal genome elimination-a type of reproduction in which males inherit but fail to pass on their father's genome-evolved independently in 6-8 arthropod clades. Thousands of species, including several important for agriculture, reproduce via this mode of reproduction. While paternal genome elimination is well established in some of the clades, the evidence in globular springtails (Symphypleona) remains elusive, even though they represent the oldest and most species-rich clade putatively reproducing via paternal genome elimination. We sequenced genomic DNA from whole bodies of Allacma fusca males with high fractions (>27.5%) of sperm to conclusively confirm that all the sperm carry 1 parental haplotype only. Although it is suggestive that the single haplotype present in sperm is maternally inherited, definitive genetic proof of the parent of origin is still needed. The genomic approach we developed allows for the detection of genotypic differences between germline and soma in all species with sufficiently high fraction of germline in their bodies. This opens new opportunities for scans of reproductive modes in small organisms.

Department of Ecological Science Faculty of Science Vrije Universiteit Amsterdam Amsterdam 1081 HV NL

Institute of Vertebrate Biology Czech Academy of Sciences 675 02 Koněšín Czech Republic

The Institute of Ecology and Evolution University of Edinburgh Edinburgh EH9 3JT UK

Zobrazit více v PubMed

Anderson N, Jaron KS, Hodson CN, Couger MB, Ševčík J, Weinstein B, Pirro S, Ross L, Roy SW.. Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems. Proc Natl Acad Sci U S A. 2022;119:e2122580119. 10.1073/pnas.2122580119 PubMed DOI PMC

Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman T-L, Hahn MW, Kitano J, Mayrose I, Ming R, et al.; Tree of Sex Consortium. Sex determination: why so many ways of doing it? PLoS Biol. 2014;12:e1001899. https://doi.org/10/gfkh5h PubMed PMC

Brown SW. Chromosomal survey of the armored and palm scale insects (Coccoidea: Diaspididae and Phoenicococcidae). Hilgardia. 1965;36:189–294.

Brun LO, Stuart J, Gaudichon V, Aronstein K, French-Constant RH.. Functional haplodiploidy: a mechanism for the spread of insecticide resistance in an important international insect pest. Proc Natl Acad Sci U S A. 1995;92:9861–9865. https://doi.org/10/b39wtm PubMed PMC

Burt A, Trivers RL.. Genes in Conflict. Cambridge: Harvard University Press; 2006.

Cannon HG. Memoirs: a further account of the spermatogenesis of lice. J Cell Sci. 1922;s2-66:657–667. https://doi.org/10/gm6t8m

Chernova NM, Potapov MB, Savenkova YuYu, Bokova AI.. Ecological significance of parthenogenesis in Collembola. Entomol Rev. 2010;90:23–38. https://doi.org/10/c97kts

Dallai R, Fanciulli PP, Carapelli A, Frati F.. Aberrant spermatogenesis and sex determination in Bourletiellidae (Hexapoda, Collembola), and their evolutionary significance. Zoomorphology. 2001;120:237–245. https://doi.org/10/c7fr66

Dallai R, Fanciulli PP, Frati F.. Chromosome elimination and sex determination in springtails (Insecta, Collembola). J Exp Zool. 1999;285:215–225. https://doi.org/10/cq83zc PubMed

Dallai R, Fanciulli PP, Frati F.. Aberrant spermatogenesis and the peculiar mechanism of sex determination in symphypleonan Collembola. J Hered. 2000;91:351–358. https://doi.org/10/dkgjmt PubMed

Dallai R, Fanciulli PP, Frati F.. New data on the aberrant spermatogenesis of Collembola. Pedobiologia. 2004;48:487–492. https://doi.org/10/bs7rmg

Dallai R, Zizzari ZV, Fanciulli PP.. Different sperm number in the spermatophores of Orchesella villosa (Geoffroy) (Entomobryidae) and Allacma fusca (L.) (Sminthuridae). Arthropod Struct Dev. 2009;38:227–234. https://doi.org/10/fk6gvz PubMed

de la Filia AG, Andrewes S, Clark JM, Ross L.. The unusual reproductive system of head and body lice (Pediculus humanus). Med Vet Entomol. 2018;32:226–234. https://doi.org/10/gf22ks PubMed PMC

de la Filia AG, Mongue AJ, Dorrens J, Lemon H, Laetsch DR, Ross L.. Males that silence their father’s genes: genomic imprinting of a complete haploid genome. Mol Biol Evol. 2021;38:2566–2581. https://doi.org/10/gm74zf PubMed PMC

Doncaster L, Cannon HG.. Memoirs: on the spermatogenesis of the louse (Pediculus corporis and P. capitis), with some observations on the maturation of the egg. J Cell Sci. 1920;s2–64:303–325. https://doi.org/10/gm6t8k

Dufresne F, Belzile C, McKindsey C, Beaudreau N.. Sperm number assessed by flow cytometry in species of Daphnia (Crustacea, Cladocera). Invertebr Biol. 2019;138:e12261. https://doi.org/10/gf759v

Faddeeva-Vakhrusheva A, Derks MFL, Anvar SY, Agamennone V, Suring W, Smit S, van Straalen NM, Roelofs D.. Gene family evolution reflects adaptation to soil environmental stressors in the genome of the Collembolan Orchesella cincta. Genome Biol Evol. 2016;8:2106–2117. https://doi.org/10/f8zg59 PubMed PMC

Fraïsse C, Picard MAL, Vicoso B.. The deep conservation of the Lepidoptera Z chromosome suggests a non-canonical origin of the W. Nat Commun. 2017;8:1486. https://doi.org/10/gcmbnr PubMed PMC

Gallun RL, Hatchett JH.. Genetic evidence of elimination of chromosomes in the Hessian Fly1,2. Ann Entomol Soc Am. 1969;62:1095–1101. https://doi.org/10/gm74zd

Garrison E, Kronenberg ZN, Dawson ET, Pedersen BS, Prins P. Vcflib and tools for processing the VCF variant call format. 2021. 10.1101/2021.05.21.445151. PubMed DOI PMC

Garrison E, Marth G. Haplotype-based variant detection from short-read sequencing. arXiv. 2012. 10.48550/arXiv.1207.3907 DOI

Gerbi SA. Unusual chromosome movements in sciarid flies. In: Hennig W, editor. Germ Line — Soma Differentiation Results and Problems in Cell Differentiation. Berlin/Heidelberg: Springer; 1986. p. 71–104. 10.1007/978-3-540-39838-7_2 PubMed DOI

Häußermann CK, Giacobino A, Munz R, Ziegelmann B, Palacio MA, Rosenkranz P.. Reproductive parameters of female Varroa destructor and the impact of mating in worker brood of Apis mellifera. Apidologie. 2020;51:342–355. https://doi.org/10/gmw43n

Helle W, Bolland HR, Heitmans WRB.. Chromosomes and types of parthenogenesis in the false spider mites (Acari: Tenuipalpidae). Genetica. 1980;54:45–50. https://doi.org/10/brsjf9

Hemmer W. Karyotype differentiation and chromosomal variability in springtails (Collembola, Insecta). Biol Fertil Soils. 1990;9:119–125. https://doi.org/10/dkqp9j

Hitchcock TJ, Gardner A, Ross L.. Sexual antagonism in haplodiploids. Evolution. 2022;76:292–309. 10.1111/evo.14398 PubMed DOI

Hodson CN, Hamilton PT, Dilworth D, Nelson CJ, Curtis CI, Perlman SJ.. Paternal genome elimination in Liposcelis booklice (Insecta: Psocodea). Genetics. 2017;206:1091–1100. https://doi.org/10/gfzgjf PubMed PMC

Hodson CN, Jaron KS, Gerbi S, Ross L.. Gene-rich germline-restricted chromosomes in black-winged fungus gnats evolved through hybridization. PLoS Biol. 2022;20:e3001559. 10.1371/journal.pbio.3001559 PubMed DOI PMC

Hopkin SP. Biology of Springtails (Insecta: Collembola). Oxford/New York: Oxford University Press; 1997.

Hoy MA. Parahaploidy of the “arrhenotokous” predator, Metaseiulus occidentalis (Acarina: Phytoseiidae) demonstrated by X-irradiation of males. Entomol Exp Appl. 1979;26:97–104. https://doi.org/10/cmjzk7

Jaron KS, Parker DJ, Anselmetti Y, Van PT, Bast J, Dumas Z, Figuet E, François CM, Hayward K, Rossier V, et al. Convergent consequences of parthenogenesis on stick insect genomes. Science advances. 2022;8(8):eabg3842. https://doi.org/10.1126/sciadv.abg3842 PubMed PMC

Jiang H, Lei R, Ding S-W, Zhu S.. Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics. 2014;15:182. https://doi.org/10/gb8wj4 PubMed PMC

Klein K, Kokko H, Ten Brink H.. Disentangling Verbal Arguments: Intralocus Sexual Conflict in Haplodiploids. Am Nat. 2021;198(6):678–693. PubMed

Kofler R, Pandey RV, Schlötterer C.. PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics. 2011;27:3435–3436. https://doi.org/10/cjmkn5 PubMed PMC

Kokot M, Długosz M, Deorowicz S.. KMC 3: counting and manipulating k-mer statistics. Bioinformatics. 2017;33:2759–2761. https://doi.org/10/f96gjp PubMed

Komaru A, Kawagishi T, Konishi K.. Cytological evidence of spontaneous androgenesis in the freshwater clam Corbicula leana Prime. Dev Genes Evol. 1998;208:46–50. https://doi.org/10/dz4n4n PubMed

Langmead B, Salzberg SL.. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–359. https://doi.org/10/gd2xzn PubMed PMC

Leo C, Carapelli A, Cicconardi F, Frati F, Nardi F.. Mitochondrial genome diversity in Collembola: phylogeny, dating and gene order. Diversity. 2019;11:169. https://doi.org/10/ggcdpd

Lohse K, Ross L.. What haplodiploids can teach us about hybridization and speciation. Mol Ecol. 2015;24:5075–5077. https://doi.org/10/f7wbwv PubMed PMC

Majtánová Z, Dedukh D, Choleva L, Adams M, Ráb P, Unmack PJ, Ezaz T.. Uniparental genome elimination in Australian carp gudgeons. Genome Biol Evol. 2021;13(6):evab030. https://doi.org/10/gnbjts PubMed PMC

McMeniman CJ, Barker SC.. Transmission ratio distortion in the human body louse, Pediculus humanus (Insecta: Phthiraptera). Heredity. 2005;96:63–68. https://doi.org/10/cd936g PubMed

Metz CW. Genetic evidence of a selective segregation of chromosomes in Sciara (Diptera). Proc Natl Acad Sci U S A. 1926;12:690–692. https://doi.org/10/d97phw PubMed PMC

Metz CW. Unisexual progenies and sex determination in Sciara. Q Rev Biol. 1931;6:306–312. https://doi.org/10/dzfwck

Metz CW. Chromosome behavior, inheritance and sex determination in Sciara. Am Nat. 1938;72:485–520. https://doi.org/10/d9nw39

Nelson-Rees WA, Hoy MA, Roush RT.. Heterochromatinization, chromatin elimination and haploidization in the parahaploid mite Metaseiulus occidentalis (Nesbitt) (Acarina: Phytoseiidae). Chromosoma. 1980;77:263–276. https://doi.org/10/cspk6x PubMed

Normark BB. The evolution of alternative genetic systems in insects. Annu Rev Entomol. 2003;48:397–423. https://doi.org/10/bggbqz PubMed

Núñez O. Cytology of Collembola. Nature. 1962;194:946–947. https://doi.org/10/bwpxxc

Patten MM, Carioscia SA, Linnen CR.. Biased introgression of mitochondrial and nuclear genes: a comparison of diploid and haplodiploid systems. Mol Ecol. 2015;24:5200–5210. https://doi.org/10/gf4ftd PubMed

Picard toolkit; Broad Institute, GitHub repository, 2019. https://broadinstitute.github.io/picard/. https://github.com/broadinstitute/picard#citing.

Porco D, Skarżyński D, Decaëns T, Hebert PDN, Deharveng L.. Barcoding the Collembola of Churchill: a molecular taxonomic reassessment of species diversity in a sub-Arctic area. Mol Ecol Resour. 2014;14:249–261. https://doi.org/10/f5svff PubMed

Ranallo-Benavidez TR, Jaron KS, Schatz MC.. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat Commun. 2020;11:1432. https://doi.org/10/ggrbdk PubMed PMC

Ross L, Shuker DM, Normark BB, Pen I.. The role of endosymbionts in the evolution of haploid-male genetic systems in scale insects (Coccoidea). Ecol Evol. 2012;2:1071–1081. https://doi.org/10/f4jdfb PubMed PMC

Schwander T, Oldroyd BP.. Androgenesis: where males hijack eggs to clone themselves. Philos Trans R Soc Lond B: Biol Sci. 2016;371:20150534. https://doi.org/10/gfxd92 PubMed PMC

Simion P, Narayan J, Houtain A, Derzelle A, Baudry L, Nicolas E, Arora R, Cariou M, Cruaud C, Gaudray FR, et al.Chromosome-level genome assembly reveals homologous chromosomes and recombination in asexual rotifer Adineta vaga. Sci Adv. 2021;7:eabg4216. 10.1126/sciadv.abg4216 PubMed DOI PMC

Stuart JJ, Hatchett JH.. Cytogenetics of the hessian fly: II. Inheritance and behavior of somatic and germ-line-limited chromosomes. J Hered. 1988;79:190–199. https://doi.org/10/gm74zb PubMed

Sulston JE, Horvitz HR.. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol. 1977;56:110–156. https://doi.org/10/b48mn4 PubMed

The Darwin Tree of Life Project Consortium. Sequence locally, think globally: The Darwin Tree of Life Project. Proc Natl Acad Sci U S A. 2022;119:e2115642118. 10.1073/pnas.2115642118 PubMed DOI PMC

Treat AE. Sex-distinctive chromatin and the frequency of males in the moth ear mite. J N Y Entomol Soc. 1965;73:12–18.

Vicoso B, Bachtrog D.. Numerous transitions of sex chromosomes in Diptera. PLoS Biol. 2015;13:e1002078. https://doi.org/10/f7crnn PubMed PMC

Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems