Abstract
Chromosome rearrangements can play an important role in adaptive evolution and speciation with gene flow. Here, we briefly review state of the art in chromosomal speciation, along with the classic model of sex chromosome evolution. The main focus lies on sex chromosome–autosome fusions, i.e., neo-sex chromosomes. We describe the presence of neo-sex chromosomes in moth and butterflies (Lepidoptera), the largest group with female heterogamety. Despite the relative stability of lepidopteran karyotypes, fusions which result either in multiple sex chromosomes (W1W2Z or WZ1Z2) or large sex chromosome pairs occurred at a surprisingly high frequency throughout their evolution. We discuss the role of meiotic drive, genetic drift, and selection in the establishing of these derived sex chromosome systems. It is hypothesized that the association between sex-linked reproductive isolation or female preference and larval performance may contribute to ecological specialization and species formation in Lepidoptera.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ahola V, Lehtonen R, Somervuo P, Salmela L, Koskinen P et al (2014) The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal fusions in Lepidoptera. Nat Commun. doi:10.1038/ncomms5737
Ayala D, Ullastres A, González J (2014) Adaptation through chromosomal inversions in Anopheles. Front Genet. doi:10.3389/fgene.2014.00129
Bachtrog D (2013) Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14(2):113–124
Baker RJ, Bickham JW (1986) Speciation by monobrachial centric fusions. P Natl Acad Sci USA 83(21):8245–8248
Bass C, Zimmer CT, Riveron JM, Wilding CS, Wondji CS et al (2013) Gene amplification and microsatellite polymorphism underlie a recent insect host shift. P Natl Acad Sci USA 110(48):19460–19465
Bellott DW, Skaletsky H, Pyntikova T, Mardis ER, Graves T et al (2010) Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466(7306):612–616
Bird CE, Fernandez-Silva I, Skillings DJ, Toonen RJ (2012) Sympatric speciation in the post “modern synthesis” era of evolutionary biology. Evol Biol 39:158–180
Brown J, Keith S, Von Schoultz B, Suomalainen E (2004) Chromosome evolution in neotropical Danainae and Ithomiinae (Lepidoptera). Hereditas 141(3):216–236
Bureš P, Zedek F (2014) Holokinetic drive: centromere drive in chromosomes without centromeres. Evolution 68(8):2412–2420
Bush GL, Case SM, Wilson AC, Patton JL (1977) Rapid speciation and chromosomal evolution in mammals. P Natl Acad Sci USA 74(9):3942–3946
Carabajal Paladino LZ, Ferrari ME, Lauría JP, Cagnotti CL, Šíchová J, López SN (2016) The effect of X-rays on cytological traits of Tuta absoluta (Lepidoptera: Gelechiidae). Fla Entomol
Charlesworth D (2013) Plant sex chromosome evolution. J Exp Bot 64(2):405–420
Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997
Charlesworth D, Charlesworth B (1980) Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet Res 35:205–214
Charlesworth B, Wall JD (1999) Inbreeding, heterozygote advantage and the evolution of neo–X and neo–Y sex chromosomes. P Roy Soc Lond B Bio 266(1414):51–56
Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95(2):118–128
De Prins J, Saitoh K (2003) Karyology and sex determination. Handbuch Der Zoologie/Handb Zool 4(36):449–468
de Villena FPM, Sapienza C (2001) Female meiosis drives karyotypic evolution in mammals. Genetics 159(3):1179–1189
Dermauw W, Osborne EJ, Clark RM, Grbić M, Tirry L et al (2013) A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae. BMC Genom. doi:10.1186/1471-2164-14-317
Edger PP, Heidel-Fischer HM, Bekaert M, Rota J, Glöckner G et al (2015) The butterfly plant arms-race escalated by gene and genome duplications. P Natl Acad Sci USA 112(27):8362–8366
Ennis TJ (1976) Sex chromatin and chromosome numbers in Lepidoptera. Can J Genet Cytol 18(1):119–130
Faria R, Navarro A (2010) Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25(11):660–669
Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78(2):737–756
Fontana PG (1976) Improved resolution of the meiotic chromosomes in both sexes of Euxoa species and their hybrids (Lepidoptera: Noctuidae). Can J Genet Cytol 18(3):537–544
Fordyce JA (2010) Host shifts and evolutionary radiations of butterflies. P Roy Soc Lond B Bio 277(1701):3735–3743
Fuková I, Nguyen P, Marec F (2005) Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome 48:1083–1092
Gassner G, Klemetson DJ (1974) A transmission electron microscope examination of hemipteran and lepidopteran gonial centromeres. Can J Genet Cytol 16(2):457–464
Guerrero RF, Kirkpatrick M (2014) Local adaptation and the evolution of chromosome fusions. Evolution 68(10):2747–2756
Hardy NB, Otto SP (2014) Specialization and generalization in the diversification of phytophagous insects: tests of the musical chairs and oscillation hypotheses. P Roy Soc Lond B Bio. doi:10.1098/rspb.2013.2960
Heckel DG, Bryson PK, Brown TM (1998) Linkage analysis of insecticide-resistant acetylcholinesterase in Heliothis virescens. J Hered 89(1):71–78
Innan H, Kondrashov F (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11(2):97–108
Ironside JE (2010) No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution. BioEssays 32(8):718–726
Kawazoé A (1987) The chromosome in the primitive or microlepidopterous moth-groups. I. Proc Japan Acad Ser B 63(6):25–28
Kitano J, Peichel CL (2012) Turnover of sex chromosomes and speciation in fishes. Environ Biol Fish 94(3):549–558
Kitano J, Ross JA, Mori S, Kume M, Jones FC et al (2009) A role for a neo-sex chromosome in stickleback speciation. Nature 461(7267):1079–1083
Lande R (1985) The fixation of chromosomal rearrangements in a subdivided population with local extinction and colonization. Heredity 54(3):323–332
Li W, Schuler MA, Berenbaum MR (2003) Diversification of furanocoumarin-metabolizing cytochrome P450 monooxygenases in two papilionids: specificity and substrate encounter rate. P Natl Acad Sci USA 100(2):14593–14598
Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253
Lohse K, Clarke M, Ritchie MG, Etges WJ (2015) Genome-wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation. Evolution 69(5):1178–1190
Lukhtanov VA (2000) Sex chromatin and sex chromosome systems in nonditrysian Lepidoptera (Insecta). J Zool Syst Evol Res 38(2):73–79
Lukhtanov V, Puplesiene J (1999) Polyploidy in bisexual Lepidoptera species (Insecta: Lepidoptera): old hypotheses and new data. Bonn Zool Beitr 48:313–328
Maeki K (1981) Notes on the W-chromosome of the butterfly, Graphium sarpedon (Papilionidae, Lepidoptera). P Jpn Acad B 57(10):371–373
Maeki K, Ae SA (1969) Studies of the chromosomes of Formosan Rhopalocera. 4. Danaidae and Satyridae. Kontyu 37(1):99–109
Mank JE, Vicoso B, Berlin S, Charlesworth B (2010) Effective population size and the Faster-X effect: empirical results and their interpretation. Evolution 64(3):663–674
Marec F, Sahara K, Traut W (2010) Rise and fall of the W chromosome in Lepidoptera. In: Goldsmith MR, Marec F (eds) Molecular biology and genetics of the Lepidoptera. CRC Press, Boca Raton, pp 49–63
Martin SH, Dasmahapatra KK, Nadeau NJ, Salazar C, Walters JR et al (2013) Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Res 23(11):1817–1828
Matsubayashi KW, Ohshima I, Nosil P (2010) Ecological speciation in phytophagous insects. Entomol Exp Appl 134(1):1–27
McAllister BF, Sheeley SL, Mena PA, Evans AL, Schlötterer C (2008) Clinal distribution of a chromosomal rearrangement: a precursor to chromosomal speciation? Evolution 62(8):1852–1865
Menken SB, Herrebout WM, Wiebes JT (1992) Small ermine moths (Yponomeuta): their host relations and evolution. Annu Rev Entomol 37:41–66
Menken SB, Boomsma JJ, Van Nieukerken EJ (2010) Large-scale evolutionary patterns of host plant associations in the Lepidoptera. Evolution 64(4):1098–1119
Murakami A, Imai HT (1974) Cytological evidence for holocentric chromosomes of the silkworms, Bombyx mori and B. mandarina (Bombycidae, Lepidoptera). Chromosoma 47(2):167–178
Nguyen P, Sýkorová M, Šíchová J, Kůta V, Dalíková M et al (2013) Neo-sex chromosomes and adaptive potential in tortricid pests. P Natl Acad Sci USA 110(17):6931–6936
Nilsson NO, Löfstedt C, Dävring L (1988) Unusual sex chromosome inheritance in six species of small ermine moths (Yponomeuta, Yponomeutidae, Lepidoptera). Hereditas 108(2):259–265
Nygren GH, Nylin S, Stefanescu C (2006) Genetics of host plant use and life history in the comma butterfly across Europe: varying modes of inheritance as a potential reproductive barrier. J Evol Biol 19(6):1882–1893
O’Meally D, Ezaz T, Georges A, Sarre SD, Graves JAM (2012) Are some chromosomes particularly good at sex? Insights from amniotes. Chromosome Res 20(1):7–19
Ohno S (1967) Sex chromosomes and sex-linked genes. Springer, Berlin
Olmo E (2005) Rate of chromosome changes and speciation in reptiles. Genetica 125(2–3):185–203
Ortiz-Barrientos D, Engelstädter J, Rieseberg LH (2016) Recombination rate evolution and the origin of species. Trends Ecol Evol 31(3):226–236
Pala I, Naurin S, Stervander M, Hasselquist D, Bensch S et al (2012) Evidence of a neo-sex chromosome in birds. Heredity 108(3):264–272
Pennell MW, Kirkpatrick M, Otto SP, Vamosi JC, Peichel CL et al (2015) Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS Genet. doi:10.1371/journal.pgen.1005237
Perrin N (2009) Sex reversal: a fountain of youth for sex chromosomes? Evolution 63(12):3043–3049
Pokorná M, Rens W, Rovatsos M, Kratochvíl L (2014) A ZZ/ZW sex chromosome system in the thick-tailed gecko (Underwoodisaurus milii; Squamata: Gekkota: Carphodactylidae), a member of the ancient gecko lineage. Cytogenet Genome Res 142(3):190–196
Potter S, Moritz C, Eldridge MDB (2015) Gene flow despite complex Robertsonian fusions among rock-wallaby(Petrogale) species. Biol Lett. doi:10.1098/rsbl.2015.0731
Presgraves DC (2002) Patterns of postzygotic isolation in Lepidoptera. Evolution 56(6):1168–1183
Prowell DP (1998) Sex linkage and speciation in Lepidoptera. In: Howards DJ, Berlocher SW (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 309–319
Rice WR (1987) The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 41(4):911–914
Robinson R (1971) Lepidoptera genetics. Pergamon Press, Oxford
Roesti M, Kueng B, Moser D, Berner D (2015) The genomics of ecological vicariance in three spine stickleback fish. Nat Commun. doi:10.1038/ncomms9767
Ross JA, Urton JR, Boland J, Shapiro MD, Peichel CL (2009) Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genet. doi:10.1371/journal.pgen.1000391
Sackton TB, Corbett-Detig RB, Nagaraju J, Vaishna L, Arunkumar KP et al (2014) Positive selection drives faster-Z evolution in silkmoths. Evolution 68(8):2331–2342
Saitoh K, Abe A (1970) On the chromosomes of five species of Danaidae from Nepal Hymalaya (Lepidoptera; Rhopalocera). Spec Bull Lep Soc Jap 4:153–158
Sharp HE, Rowell DM (2007) Unprecedented chromosomal diversity and behaviour modify linkage patterns and speciation potential: structural heterozygosity in an Australian spider. J Evol Biol 20(6):2427–2439
Šíchová J, Nguyen P, Dalíková M, Marec F (2013) Chromosomal evolution in tortricid moths: conserved karyotypes with diverged features. PLoS ONE. doi:10.1371/journal.pone.0064520
Šíchová J, Voleníková A, Dincă V, Nguyen P, Vila R et al (2015) Dynamic karyotype evolution and unique sex determination systems in Leptidea wood white butterflies. BMC Evol Biol. doi:10.1186/s12862-015-0375-4
Šíchová J, Ohno M, Dincă V, Watanabe M, Sahara K et al (2016) Fissions, fusions, and translocations shaped the karyotype and multiple sex chromosome constitution of the northeast Asian wood white butterfly, Leptidea amurensis. Biol J Linn Soc 118(3):457–47
Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L et al (2003) The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423(6942):825–837
Smadja CM, Butlin RK (2011) A framework for comparing processes of speciation in the presence of gene flow. Mol Ecol 20:5123–5140
Sohn JC, Regier JC, Mitter C, Davis D, Landry JF et al (2013) A molecular phylogeny for Yponomeutoidea (Insecta, Lepidoptera, Ditrysia) and its implications for classification, biogeography and the evolution of host plant use. PLoS ONE. doi:10.1371/journal.pone.0055066
Sohn JC, Rregier JC, Mitter C, Adamski D, Landry JF et al (2015) Phylogeny and feeding trait evolution of the mega-diverse Gelechioidea (Lepidoptera: Obtectomera): new insight from 19 nuclear genes. Syst Entomol. doi:10.1111/syen.12143
Sperling FA (1994) Sex-linked genes and species differences in Lepidoptera. Can Entomol 126(03):807–818
Suomalainen E (1969) On the sex chromosome trivalent in some Lepidoptera females. Chromosoma 28(3):298–308
Suomalainen E (1971) Unequal sex chromosomes in a moth, Lozotaenia forsterana F. (Lepidoptera: Tortricidae). Hereditas 68(2):313–315
Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47(1):3–14
Traut W, Marec F (1996) Sex chromatin in Lepidoptera. Q Rev Biol 71(2):239–256
Traut W, Marec F (1997) Sex chromosome differentiation in some species of Lepidoptera (Insecta). Chromosome Res 5(5):283–291
Traut W, Sahara K, Marec F (2007) Sex chromosomes and sex determination in Lepidoptera. Sex Dev 1(6):332–346
Turner H, Lieshout N, Van Ginkel WE, Menken SB (2010) Molecular phylogeny of the small ermine moth genus Yponomeuta (Lepidoptera, Yponomeutidae) in the Palaearctic. PloS ONE. doi:10.1371/journal.pone.0009933
van Nieukerken EJ, Kaila L, Kitching IJ, Kristensen NP, Lees DJ et al (2011) Order Lepidoptera Linnaeus, 1758. Zootaxa 3148:212–221
Van’t Hof AE, Nguyen P, Dalíková M, Edmonds N, Marec F et al (2013) Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism. Heredity 110(3):283–295
Veltsos P, Keller I, Nichols RA (2008) The inexorable spread of a newly arisen neo-Y chromosome. PLoS Genet. doi:10.1371/journal.pgen.1000082
Vicoso B, Bachtrog D (2013) Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature 499(7458):332–335
Vicoso B, Emmerson JJ, Zektser Y, Mahajan S, Bachtrog D (2013) Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol. doi:10.1371/journal.pbio.1001643
Vítková M, Fuková I, Kubíčková S, Marec F (2007) Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosome Res 15(7):917–930
Walters J, Mongue AJ (2016) A neo-sex chromosome in the Monarch butterfly, Danaus plexippus. bioRxiv. doi:10.1101/036483
White MJD (1973) Animal cytology and evolution. Cambridge University Press, Cambridge
Wolf KW (1994) The unique structure of lepidopteran spindles. Int Rev Cytol 152:1–48
Xie X, Cheng T, Wang G, Duan J, Niu W et al (2012) Genome-wide analysis of the ATP-binding cassette (ABC) transporter gene family in the silkworm, Bombyx mori. Mol Biol Rep 39(7):7281–7291
Yeaman S (2013) Genomic rearrangements and the evolution of clusters of locally adaptive loci. Proc Natl Acad Sci USA 110(19):E1743–E1751
Yoshida K, Kitano J (2012) The contribution of female meiotic drive to the evolution of neo-sex chromosomes. Evolution 66(10):3198–3208
Yoshida K, Makino T, Yamaguchi K, Shigenobu S, Hasebe M et al (2014) Sex chromosome turnover contributes to genomic divergence between incipient stickleback species. PLoS Genet. doi:10.1371/journal.pgen.1004223
Yoshido A, Marec F, Sahara K (2005) Resolution of sex chromosome constitution by genomic in situ hybridization and fluorescence in situ hybridization with (TTAGG)n telomeric probe in some species of Lepidoptera. Chromosoma 114:193–202
Yoshido A, Sahara K, Marec F, Matsuda Y (2011) Step-by-step evolution of neo-sex chromosomes in geographical populations of wild silkmoths, Samia cynthia ssp. Heredity 106(4):614–624
Yoshido A, Šíchová J, Kubíčková S, Marec F, Sahara K (2013) Rapid turnover of the W chromosome in geographical populations of wild silkmoths, Samia cynthia ssp. Chromosome Res 21(2):149–164
Yu QY, Lu C, Li WL, Xiang ZH, Zhang Z (2009) Annotation and expression of carboxylesterases in the silkworm, Bombyx mori. BMC Genomics. doi:10.1186/1471-2164-10-553
Zangerl AR, Liao LH, Jogesh T, Berenbaum MR (2012) Aliphatic esters as targets of esterase activity in the parsnip webworm (Depressaria pastinacella). J Chem Ecol 38(2):188–194
Acknowledgements
We thank Alexander Barton, Anna Voleníková, Atsuo Yoshido, Irena Hladová, Jindra Šíchová, Magda Zrzavá, Martina Dalíková, and Sander Visser for their critical reading of the manuscript. The present chapter was supported by Grants 14-35819P and 16-10298S of the Czech Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2016 Springer International Publishing Switzerland
About this chapter
Cite this chapter
Nguyen, P., Carabajal Paladino, L. (2016). On the Neo-Sex Chromosomes of Lepidoptera. In: Pontarotti, P. (eds) Evolutionary Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-41324-2_11
Download citation
DOI: https://doi.org/10.1007/978-3-319-41324-2_11
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-41323-5
Online ISBN: 978-3-319-41324-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)