Abstract
The stick-insect genus Pijnackeria includes four diploid bisexual and two polyploid (3n, 4n) parthenogenetic species. Earlier analyses of the tetraploid parthenogen P. hispanica using mitochondrial markers allowed tracing its maternal ancestry to Pijnackeria originis, while no maternal nuclear contribution was found, thus suggesting an androgenetic and hybrid origin. The recently described Pijnackeria recondita—showing, among other features, a specific antennal structure linking it to the tetraploid parthenogen—prompted us to check whether the new species could be the unknown paternal ancestor of P. hispanica. In this work, we use karyology and molecular analysis of the mitochondrial gene cytochrome c oxidase subunit 2 (cox2) and the nuclear gene elongation factor 1 subunit α (ef1-α) to investigate the origin of such a complex tetraploid hybrid parthenogen. The molecular analysis supported P. recondita as being a paternal ancestor of P. hispanica, but also suggested that two more fathering species have to be taken into account: P. barbarae and the unknown paternal ancestor of the triploid hybrid P. masettii. Therefore, P. hispanica is apparently a polyphyletic chimeric androgen, which we propose to indicate as an androgenetic complex. Our data also revealed that P. hispanica is between 1.96 Myr and 3.31 Myr old, making it the oldest parthenogenetic taxon discovered among insects.
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References
Bell, G. (1982). Masterpiece of nature: the evolution and genetics of sexuality. London: Croom Helm.
Bianchi, A. (1992). Karyological studies of Mediterranean stick-insects belonging to the genera Clonopsis and Leptynia (Insecta Phasmatodea). Caryologia, 45(1), 1–19. https://doi.org/10.1080/00087114.1992.10797205.
Bianchi, A., & Meliadò, P. (1998). Analysis of the karyotypes of four species of the Leptynia attenuata complex (Insecta Phasmatodea). Caryologia, 51(3–4), 207–219. https://doi.org/10.1080/00087114.1998.10797413.
Bonandin, L., Scavariello, C., Luchetti, A., Mantovani, B. (2014). Evolutionary dynamics of R2 retroelement and insertion inheritance in the genome of bisexual and parthenogenetic populations (Insecta Phasmida). Insect Molecular Biology, 23(6), 808–820.
Bonandin, L., Scavariello, C., Mingazzini, V., Luchetti, A., Mantovani, B. (2017). Obligatory parthenogenesis and TE load: stick insects and the R2 non-LTR retrotransposon. Insect Science, 24(3), 409–417.
Brock, P. (1991). Stick-insects of Britain, Europe and the Mediterranean. London: Fitzgerald Publishing.
Brock, P. D. (1993). Studies on stick insects of the genus Leptynia in Spain. Amateur Entomologist’s Society Bulletin, 52, 165–172.
Byrne, M., Phelps, H., Church, T., Adair, V., Selvakumaraswamy, P., & Potts, J. (2000). Reproduction and development of the freshwater clam Corbicula australis in Southeast Australia. Hydrobiologia, 418, 185–197. https://doi.org/10.1023/A:1003986512832.
Clement, M., Posada, D., & Crandall, K. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9(10), 1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x.
Craddock, E. (1972). Chromosomal diversity in the Australian Phasmatodea. Australian Journal of Zoology, 20(4), 445–462. https://doi.org/10.1071/zo9720445.
Craddock, E. (1975). Intraspecific karyotypic differentiation in the Australian phasmatid Didymuria violescens (leach). Chromosoma, 53(1), 1–24. https://doi.org/10.1007/bf00329387.
Drummond, A., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7(1), 214. https://doi.org/10.1186/1471-2148-7-214.
Ghiselli, F., Milani, L., Scali, V., & Passamonti, M. (2007). The Leptynia hispanica species complex (Insecta Phasmida): polyploidy, parthenogenesis, hybridization and more. Molecular Ecology, 16(20), 4256–4268. https://doi.org/10.1111/j.1365-294x.2007.03471.x.
John, B., Rentz, D., & Contreras, N. (1987). Extensive chromosome variation in the stick insect genus Sipyloidea Brunner von Wattenwyl (Phylliidae : Necrosciinae) within Australia, and descriptions of three new species. Invertebrate Systematics, 1(6), 603–630. https://doi.org/10.1071/it9870603.
Komaru, A., Kawagishi, T., & Konishi, K. (1998). Cytological evidence of spontaneous androgenesis in the freshwater clam Corbicula leana prime. Development Genes and Evolution, 208(1), 46–50. https://doi.org/10.1007/s004270050152.
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870–1874. https://doi.org/10.1093/molbev/msw054.
Liehr, T., Buleu, O., Karamysheva, T., Bugrov, A., Rubtsov, N., (2017). New Insights into Phasmatodea Chromosomes. Genes, 8(11):327.
Manaresi, S., Marescalchi, O., & Scali, V. (1991). Ag-detected NOR and C-banding patterns in Bacillus rossius (Insecta Phasmatodea) from Sicily. Caryologia, 44(3–4), 265–286. https://doi.org/10.1080/00087114.1991.10797192.
Manaresi, S., Marescalchi, O., & Scali, V. (1992a). The chromosome complement of the hybrid Bacillus whitei complex (Insecta Phasmatodea). I. The paleo- and neo-standard karyotypes. Cytologia, 57(1), 101–109. https://doi.org/10.1508/cytologia.57.101.
Manaresi, S., Marescalchi, O., & Scali, V. (1992b). The chromosome complement of the hybrid Bacillus whitei complex (Insecta Phasmatodea). II. The repatterned cytotypes. Cytologia, 57(1), 111–119. https://doi.org/10.1508/cytologia.57.111.
Manaresi, S., Marescalchi, O., & Scali, V. (1993). The trihybrid genome constitution of Bacillus lynceorum (Insecta Phasmatodea) and its karyotypic variations. Genome, 36(2), 317–326. https://doi.org/10.1139/g93-044.
Mantovani, B., & Scali, V. (1992). Hybridogenesis and androgenesis in the stick-insect Bacillus rossius-grandii benazzii (Insecta, Phasmatodea). Evolution, 46(3), 783–796. https://doi.org/10.2307/2409646.
Mantovani, B., Passamonti, M., & Scali, V. (2001). The mitochondrial cytochrome oxidase II gene in Bacillus stick insects: ancestry of hybrids, androgenesis, and phylogenetic relationships. Molecular Phylogenetics and Evolution, 19(1), 157–163. https://doi.org/10.1006/mpev.2000.0850.
Marescalchi, O., & Scali, V. (1997). Chromosomal and NOR patterns in the polyclonal stick insect Bacillus atticus atticus (Insecta; Phasmatodea). Genome, 40(2), 261–270. https://doi.org/10.1139/g97-037.
Marescalchi, O., & Scali, V. (2003). Automictic parthenogenesis in the diploid-triploid stick insect Bacillus atticus and its flexibility leading to heterospecific diploid hybrids. Invertebrate Reproduction and Development, 43(2), 163–172. https://doi.org/10.1080/07924259.2003.9652535.
Marescalchi, O., Pijnacker, L., & Scali, V. (1991). Cytology of parthenogenesis in Bacillus whitei and Bacillus lynceorum (Insecta Phasmatodea). Invertebrate Reproduction and Development, 20(1), 75–81. https://doi.org/10.1080/07924259.1991.9672180.
Meyne, J., Baker, R., Hobart, H., Hsu, T., Ryder, O., Ward, O., et al. (1990). Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma, 99(1), 3–10. https://doi.org/10.1007/bf01737283.
Milani, L., Scali, V., & Passamonti, M. (2009). The Clonopsis gallica puzzle: Mendelian species, polyploid parthenogens with karyotype re-diploidization and clonal androgens in Moroccan stick insects (Phasmida). Journal of Zoological Systematics and Evolutionary Research, 47(2), 132–140. https://doi.org/10.1111/j.1439-0469.2008.00489.x.
Milani, L., Ghiselli, F., Pellecchia, M., Scali, V., & Passamonti, M. (2010). Reticulate evolution in stick insects: the case of Clonopsis (Insecta Phasmida). BMC Evolutionary Biology, 10(1), 258. https://doi.org/10.1186/1471-2148-10-258.
Milani, L., Scali, V., & Passamonti, M. (2014). Speciation through androgenesis in the stick insect genus Clonopsis (Insecta Phasmatodea). Journal of Zoological Systematics and Evolutionary Research, 53(2), 116–123. https://doi.org/10.1111/jzs.12087.
Normark, B., Judson, O., & Moran, N. (2003). Genomic signatures of ancient asexual lineages. Biological Journal of the Linnean Society, 79(1), 69–84. https://doi.org/10.1046/j.1095-8312.2003.00182.x.
Ocalewicz, K. (2013). Telomeres in Fishes. Cytogenetic and Genome Research, 141 (2–3):114–125.
Pantel, P. J. (1890). Notes Orthoptérologiques II Les Phasmides d’Europe et des pays limitrophes. Anales Sociedad Española de Historia Natural, 19, 371–404.
Pichot, C., El Maâtaoui, M., Raddi, S., & Raddi, P. (2001). Surrogate mother for endangered Cupressus. Nature, 412(6842), 39. https://doi.org/10.1038/35083687.
Preiss, A., Hartley, D., & Artavanis-Tsakonas, S. (1988). The molecular genetics of enhancer of split, a gene required for embryonic neural development in Drosophila. The EMBO Journal, 7(12), 3917–3927. https://doi.org/10.1002/j.1460-2075.1988.tb03278.x.
Qiu, A. D., Shi, A. J., & Komaru, A. (2001). Yellow and brown shell color morphs of Corbicula fluminea (Bivalvia: Corbiculidae) from Sichuan Province, China, are triploids and tetraploids. Journal of Shellfish Research, 20, 323–328.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542. https://doi.org/10.1093/sysbio/sys029.
Ruiz-Herrera, A., Nergadze, S., Santagostino, M., & Giulotto, E. (2008). Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenetic and Genome Research, 122(3–4), 219–228. https://doi.org/10.1159/000167807.
Salvadori, S., Coluccia, E., Deidda, F., Sibiriu, M., Costa, E., Deiana, A. M., & Scali, V. (2018). Multiple highly amplified NORs co-localized with telomeric sequences in the parthenogenetic hybrid Bacillus whitei (Insecta Phasmatodea). Comparative Cytogenetics, 12(3), 299–360. https://doi.org/10.3897/CompCytogen.v12i3.27748.
Satović, E., Vojvoda Zeljko, T., Luchetti, A., Mantovani, B., & Plohl, M. (2016). Adjacent sequences disclose potential for intra-genomic dispersal of satellite DNA repeats and suggest a complex network with transposable elements. BMC Genomics, 17(1), 997. https://doi.org/10.1186/s12864-016-3347-1.
Scali, V. (1972). La citologia della partenogenesi di Bacillus rossius. Bollettino di Zoologia, 39(4), 567–573. https://doi.org/10.1080/11250007209431412.
Scali, V. (2009a). Metasexual stick insects: model pathways to losing sex and bringing it back. In I. Schön, K. Martens, & P. Dijk (Eds.), Lost sex. Dordrecht: Springer. https://doi.org/10.1007/978-90-481-2770-2_16.
Scali, V. (2009b). Revision of the Iberian stick insect genus Leptynia Pantel and description of the new genus Pijnackeria. The Italian Journal of Zoology, 76(4), 381–391. https://doi.org/10.1080/11250000802702062.
Scali, V., Deidda, F., Coluccia, E., Melis, R., Cannas, R., & Salvadori, S. (2020). Parental species and hybrid descendants of Bacillus (Insecta Phasmatodea) show different patterns of highly amplified, colocalized ribosomal and telomeric sequences. The European Zoological Journal (proofs).
Scali, V., Tinti, F., Mantovani, B., & Marescalchi, O. (1995). Mate recognition and gamete cytology features allow hybrid species production and evolution in Bacillus stick insects. Bollettino di Zoologia, 62(1), 59–70. https://doi.org/10.1080/11250009509356052.
Scali, V., Milani, L., & Passamonti, M. (2010). Clonopsis gallica, a stick insect parthenogen exploiting different egg maturation mechanisms over its range. Invertebrate Reproduction and Development, 54(3), 143–150. https://doi.org/10.1080/07924259.2010.9652326.
Scali, V., Milani, L., & Passamonti, M. (2012). Revision of the stick insect genus Leptynia: description of new taxa, speciation mechanism and phylogeography. Contributions to Zoology, 81(1), 25–42.
Scali, V., Milani, L., & Passamonti, M. (2013). Description and ecology of new Pijnackeria stick insects: four bisexual species and a triploid parthenogen with their phyletic relationships. Journal of Zoological Systematics and Evolutionary Research, 51(3), 213–226. https://doi.org/10.1111/jzs.12018.
Scali, V., Coluccia, E., Deidda, F., Lobina, C., Deiana, A., & Salvadori, S. (2016). Co-localization of ribosomal and telomeric sequences in Leptynia (Insecta: Phasmatodea). The Italian Journal of Zoology, 83(3), 285–290. https://doi.org/10.1080/11250003.2016.1219403.
Scavariello, C., Luchetti, A., Martoni, F., Bonandin, L., & Mantovani, B. (2017). Hybridogenesis and a potential case of R2 non-LTR retrotransposon horizontal transmission in Bacillus stick insects (Insecta Phasmida). Scientific Reports, 7(1), 41946. https://doi.org/10.1038/srep41946.
Schwander, T., Henry, L., & Crespi, B. (2011). Molecular evidence for ancient asexuality in Timema stick insects. Current Biology, 21(13), 1129–1134. https://doi.org/10.1016/j.cub.2011.05.026.
Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312–1313. https://doi.org/10.1093/bioinformatics/btu033.
Taddei, C., Maurizii, M., Chicca, M., & Scali, V. (1993). The germarium of panoistic ovarioles of Bacillus rossius (Insecta Phasmatodea): structure and function during imaginal life. Invertebrate Reproduction and Development, 23(2–3), 203–210. https://doi.org/10.1080/07924259.1993.9672316.
Tinti, F., & Scali, V. (1996). Androgenetics and triploids from an interacting parthenogenetic hybrid and its ancestors in stick insects. Evolution, 50(3), 1251–1258. https://doi.org/10.2307/2410665.
Valero, P., & Ortiz, A. S. (2015). Description and DNA barcoding of a new Iberian species of Pijnackeria (Scali, 2009) from the Sierra Nevada, Spain (Phasmida: Diapheromeridae). Zootaxa, 4058(4), 535–550. https://doi.org/10.11646/zootaxa.4058.4.5.
Vrijenhoek, R. (1998). Animal clones and diversity. Bioscience, 48(8), 617–628. https://doi.org/10.2307/1313421.
Vrijenhoek, R., & Lerman, S. (1982). Heterozygosity and developmental stability under sexual and asexual breeding systems. Evolution, 36(4), 768–776. https://doi.org/10.2307/2407890.
Zhdanova, N., Rubtsov, N., & Minina, Y. (2007). Terminal regions of mammal chromosomes: plasticity and role in evolution. Russian Journal of Genetics, 43(7), 721–732. https://doi.org/10.1134/s1022795407070022.
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We would like to thank Luciana Eliopoli for the Sierra Nevada sample collection.
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This work was supported by the Canziani bequest.
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Milani, L., Scali, V., Punzi, E. et al. The puzzling taxonomic rank of Pijnackeria hispanica, a chimerical hybrid androgen (Insecta, Phasmida). Org Divers Evol 20, 285–297 (2020). https://doi.org/10.1007/s13127-020-00436-1
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DOI: https://doi.org/10.1007/s13127-020-00436-1