Parthenogenesis in animals is often associated with polyploidy and restriction to extreme habitats or recently deglaciated areas. It has been hypothesized that benefits conferred by asexual reproduction and polyploidy are essential for colonizing these habitats. However, while evolutionary routes to parthenogenesis are manifold, study systems including polyploids are scarce in arthropods. The jumping-bristletail genus Machilis (Insecta: Archaeognatha) includes both sexual and parthenogenetic species, and recently, the occurrence of polyploidy has been postulated. Here, we applied flow cytometry, karyotyping, and mitochondrial DNA sequencing to three sexual and five putatively parthenogenetic Eastern-Alpine Machilis species to investigate whether (1) parthenogenesis originated once or multiply and (2) whether parthenogenesis is strictly associated with polyploidy. The mitochondrial phylogeny revealed that parthenogenesis evolved at least five times independently among Eastern-Alpine representatives of this genus. One parthenogenetic species was exclusively triploid, while a second consisted of both diploid and triploid populations. The three other parthenogenetic species and all sexual species were diploid. Our results thus indicate that polyploidy can co-occur with parthenogenesis, but that it was not mandatory for the emergence of parthenogenesis in Machilis. Overall, we found a weak negative correlation of monoploid genome size (Cx) and chromosome base number (x), and this connection is stronger among parthenogenetic species alone. Likewise, monoploid genome size decreased with elevation, and we therefore hypothesize that genome downsizing could have been crucial for the persistence of alpine Machilis species. Finally, we discuss the evolutionary consequences of intraspecific chromosomal rearrangements and the presence of B chromosomes. In doing so, we highlight the potential of Alpine Machilis species for research on chromosomal and genome-size alterations during speciation.

Institute of Botany University of Innsbruck Sternwartestraße 15 Innsbruck 6020 Austria

Institute of Ecology University of Innsbruck Technikerstraße 25 Innsbruck 6020 Austria

Institute of Entomology Biology Centre ASCR Branisovska 31 Ceské Budejovice 37005 Czech Republic

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Adolfsson S, Michalakis Y, Paczesniak D, Bode SNS, Butlin RK, Lamatsch DK, et al. Evaluation of elevated ploidy and asexual reproduction as alternative explanations for geographic parthenogenesis in Eucypris virens ostracods. Evolution. 2010;64:986–997. PubMed

Bell G. The masterpiece of nature: the evolution and genetics of sexuality. Berkeley: Univ. of California Press; 1982.

Bengtsson BO. Asex and evolution: a very large-scale overview. In: Schön I, Martens K, Dijk PV, editors. Lost sex. Dordrecht, The Netherlands: Springer; 2009. pp. 1–19.

Blackman RL, Spence JM, Normark BB. High diversity of structurally heterozygous karyotypes and rDNA arrays in parthenogenetic aphids of the genus Trama (Aphididae: Lachninae) Heredity. 2000;84:254–260. PubMed

Bode SNS, Adolfsson S, Lamatsch DK, Martins MJF, Schmit O, Vandekerkhove J, et al. Exceptional cryptic diversity and multiple origins of parthenogenesis in a freshwater ostracod. Mol. Phylogenet. Evol. 2010;54:542–552. PubMed

Camacho JPM. B chromosomes. In: Gregory TR, editor. The evolution of the genome. Burlington, MA, USA: Elsevier Academic Press; 2005. pp. 223–286.

Castiglia R. Sympatric sister species in rodents are more chromosomally differentiated than allopatric ones: implications for the role of chromosomal rearrangements in speciation. Mamm. Rev. 2014;44:1–4.

Choleva L, Janko K. Rise and persistence of animal polyploidy: evolutionary constraints and potential. Cytogenet. Genome Res. 2013;140:151–170. PubMed

Comai L. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 2005;6:836–846. PubMed

Cuellar O. Animal parthenogenesis. Science. 1977;197:837–843. PubMed

Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods. 2012;9:772. PubMed PMC

Dejaco T, Arthofer W, Sheets HD, Moder K, Thaler-Knoflach B, Christian E, et al. A toolbox for integrative species delimitation in Machilis jumping bristletails (Microcoryphia: Machilidae) Zoologischer Anzeiger - J. Comp. Zool. 2012;251:307–316.

Elzinga J, Jokela J, Shama LN. Large variation in mitochondrial DNA of sexual and parthenogenetic Dahlica triquetrella (Lepidoptera: Psychidae) shows multiple origins of parthenogenesis. BMC Evol. Biol. 2013;13:90. PubMed PMC

Ghiselli F, Milani L, Scali V, Passamonti M. The Leptynia hispanica species complex (Insecta Phasmida): polyploidy, parthenogenesis, hybridization and more. Mol. Ecol. 2007;16:4256–4268. PubMed

Glesener RR, Tilman D. Sexuality and the components of environmental uncertainty: clues from geographic parthenogenesis in terrestrial animals. Am. Nat. 1978;112:659–673.

Gould SJ. Dollo on Dollo's law: irreversibility and the status of evolutionary laws. J. Hist. Biol. 1970;3:189–212. PubMed

Gregory TR. Animal genome size database. 2014. http://www.genomesize.com.

Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003;52:696–704. PubMed

Hessen DO, Jeyasingh PD, Neiman M, Weider LJ. Genome streamlining and the elemental costs of growth. Trends Ecol. Evol. 2010;25:75–80. PubMed

Hörandl E. Geographic parthenogenesis: opportunities for asexuality. In: Schön I, Martens K, Dijk PV, editors. Lost sex - the evolutionary biology of parthenogenesis. Dordrecht: Springer; 2009. pp. 161–186.

Houben A, Banaei-Moghaddam A, Klemme S, Timmis J. Evolution and biology of supernumerary B chromosomes. Cell. Mol. Life Sci. 2014;71:467–478. PubMed PMC

Janetschek H. Beitrag zur Kenntnis der Felsenspringer (Thysanura, Machilidae) Nordtirols. Veröffentlichungen des Museums Ferdinandeum (Innsbruck) 1949;26/29:147–165.

Janetschek H. Über mitteleuropäische Felsenspringer (Ins., Thysanura) Österreichische Zoologische Zeitschrift. 1954;5:281–328.

Janetschek H. Das Problem der inneralpinen Eiszeitüberdauerung durch Tiere (Ein Beitrag zur Geschichte der Nivalfauna) Österreichische Zoologische Zeitschrift. 1956;6:421–506.

Johnston JS, Bennett MD, Rayburn AL, Galbraith DW, Price HJ. Reference standards for determination of DNA content of plant nuclei. Am. J. Bot. 1999;86:609–613. PubMed

Judson OP, Normark BB. Ancient asexual scandals. Trends Ecol. Evol. 1996;11:41–46. PubMed

Kearney M. Why is sex so unpopular in the Australian desert? Trends Ecol. Evol. 2003;18:605–607.

Kearney M. Hybridization, glaciation and geographical parthenogenesis. Trends Ecol. Evol. 2005;20:495–502. PubMed

Kratochvíl J. Naše supinušky se zvláštnim zřetelem na moravská chránĕná území. Folia Entomologica. 1945;8:41–67.

Law JH, Crespi BJ. The evolution of geographic parthenogenesis in Timema walking-sticks. Mol. Ecol. 2002;11:1471–1489. PubMed

Leitch IJ, Bennett MD. Genome downsizing in polyploid plants. Biol. J. Linn. Soc. 2004;82:651–663.

Lundmark M, Saura A. Asexuality alone does not explain the success of clonal forms in insects with geographical parthenogenesis. Hereditas. 2006;143:23–32. PubMed

Mable BK. ‘Why polyploidy is rarer in animals than in plants’: myths and mechanisms. Biol. J. Linn. Soc. 2004;82:453–466.

Maccari M, Amat F, Gómez A. Origin and genetic diversity of diploid parthenogenetic Artemia in Eurasia. PLoS ONE. 2013;8:e83348. PubMed PMC

Maniatsi S, Baxevanis AD, Kappas I, Deligiannidis P, Triantafyllidis A, Papakostas S, et al. Is polyploidy a persevering accident or an adaptive evolutionary pattern? The case of the brine shrimp Artemia. Mol. Phylogenet. Evol. 2011;58:353–364. PubMed

Manriquez-Moran NL, Cruz FR, Murphy RW. Genetic variation and origin of parthenogenesis in the Aspidoscelis cozumela complex: evidence from mitochondrial genes. Zoolog. Sci. 2014;31:14–19. PubMed

Maynard Smith J. The evolution of sex. Cambridge, UK: Cambridge Univ. Press; 1978.

Otto SP, Whitton J. Polyploid incidence and evolution. Annu. Rev. Genet. 2000;34:401–437. PubMed

Palissa A. Apterygota. Leipzig: Quelle & Meyer; 1964.

Reeves AAJT. 2000. MicroMeasure for Windows, version 3.3 , Free program distributed by the authors over the Internet from http://www.colostate.edu/Depts/Biology/MicroMeasure.

Riezler H. Über Machiliden Nordtirols. Veröffentlichungen des Museums Ferdinandeum (Innsbruck) 1941;19:193–267.

Rinnhofer L, Roura-Pascual N, Arthofer W, Dejaco T, Thaler-Knoflach B, Wachter G, et al. Iterative species distribution modelling and ground validation in endemism research: an Alpine jumping bristletail example. Biodivers. Conserv. 2012;21:2845–2863.

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. PubMed PMC

Sahara K, Marec F, Traut W. TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res. 1999;7:449–460. PubMed

Schönswetter P, Suda J, Popp M, Weiss-Schneeweiss H, Brochmann C. Circumpolar phylogeography of Juncus biglumis (Juncaceae) inferred from AFLP fingerprints, cpDNA sequences, nuclear DNA content and chromosome numbers. Mol. Phylogenet. Evol. 2007;42:92–103. PubMed

Schwander T, Crespi BJ. Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects. Evolution. 2009;63:84–103. PubMed

Stenberg P, Lundmark M, Knutelski S, Saura A. Evolution of clonality and polyploidy in a weevil system. Mol. Biol. Evol. 2003;20:1626–1632. PubMed

Suda J, Weiss-Schneeweiss H, Tribsch A, Schneeweiss GM, Trávnícek P, Schönswetter P. Complex distribution patterns of di-, tetra-, and hexaploid cytotypes in the European high mountain plant Senecio carniolicus (Asteraceae) Am. J. Bot. 2007;94:1391–1401. PubMed

Sunnucks P, Chisholm D, Turak E, Hales DF. Evolution of an ecological trait in parthenogenetic Sitobion aphids. Heredity. 1998;81:638–647.

Suomalainen E. Polyploidy in parthenogenetic Curculionidae. Hereditas. 1940;26:51–64.

Suomaleinen E, Saura A, Lokki J. Cytology and evolution in parthenogenesis. Boca Raton, FL: CRC Press Inc; 1987.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011;28:2731–2739. PubMed PMC

Trivers R, Burt A, Palestis BG. B chromosomes and genome size in flowering plants. Genome. 2004;47:1–8. PubMed

Vandel A. La parthénogenèse géographique: Contribution à l'étude biologique et cytologique de la parthénogenèse naturelle. Bulletin biologique de la France et de la Belgique. 1928;62:164–281.

Vrijenhoek RC. Geographical parthenogenesis: General purpose genotypes and frozen niche variation. In: Schön I, Martens K, Dijk PV, Parker ED Jr, editors. Lost sex. Dordrecht, The Netherlands: Springer; 2009. pp. 99–131.

Wachter GA, Arthofer W, Dejaco T, Rinnhofer LJ, Steiner FM, Schlick-Steiner BC. Pleistocene survival on central Alpine nunataks: genetic evidence from the jumping bristletail Machilis pallida. Mol. Ecol. 2012;21:4983–4995. PubMed

Wygodzinsky PW. Beiträge zur Kenntnis der Dipluren und Thysanuren der Schweiz. Denkschriften der Schweizerischen Naturforschenden Gesellschaft. 1941;74:110–227.

Zhang L, Lefcort H. The effects of ploidy level on the thermal distributions of brine shrimp Artemia parthenogenetica and its ecological implications. Heredity. 1991;66:445–452.

Molecular cytogenetic analysis of a triploid population of the human broad tapeworm, Dibothriocephalus latus (Diphyllobothriidea)

Karyotype Variability and Inter-Population Genomic Differences in Freshwater Ostracods (Crustacea) Showing Geographical Parthenogenesis