Abstract
The evolution of genome size has been discussed in relation to the evolution of various biological traits. In the present study, the genome sizes of 22 dictyopteran species were estimated by Feulgen image analysis densitometry and 6-diamidino-2-phenylindole (DAPI)-based flow cytometry. The haploid genome sizes (C-values) of termites (Isoptera) ranged from 0.58 to 1.90 pg, and those of Cryptocercus wood roaches (Cryptocercidae) were 1.16 to 1.32 pg. Compared to known values of other cockroaches (Blattaria) and mantids (Mantodea), these values are low. A relatively small genome size appears to be a (syn)apomorphy of Isoptera + Cryptocercus, together with their sociality. In some phylogenetic groups, genome size evolution is thought to be influenced by selective pressure on a particular trait, such as cell size or rate of development. The present results raise the possibility that genome size is influenced by selective pressures on traits associated with the evolution of sociality.
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References
Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches: ecology, behavior, and natural history. Johns Hopkins University Press, Baltimore, Maryland, p 230
Bennett MD, Leitch IJ, Price HJ, Johnston JS (2003) Comparisons with Caenorhabditis (~100 Mb) and Drosophila (~175 Mb) using flow cytometry show genome size in Arabidopsis to be ~157 Mb and thus ~25% larger than the Arabidopsis genome size initiative estimate of ~125 Mb. Ann Bot 91:547–557
Bier K, Müller W (1969) DNA-messungen bei insekten und eine hypothese über retardierte evolution und besonderen DNA-reichtum in tierreich. Biol Zent bl 88:425–449
Cavalier-Smith T (1985) Introduction: the evolutionary significance of genome size. In: Cavalier-Smith T (ed) The evolution of genome size. Wiley, Chichester, UK, pp 1–36
Cornette R, Koshikawa S, Hojo M, Matsumoto T, Miura T (2006) A caste-specific cytochrome P450 in the damp-wood termite Hodotermopsis sjostedti (Isoptera, Termopsidae). Insect Mol Biol 15:235–244
Costa JT (2006) The other insect societies. The Belknap Press of Harvard University Press, Cambridge, Massachusetts, p 812
Crozier RH (2004) The other core eusocial insects: a need for termite genomics. In: Entomology Strength in Diversity: Proceedings of XXII International Congress of Entomology (with CD-ROM). Brisbane, Australia, p 161, section 18 in CD-ROM
Deitz LL, Nalepa C, Klass K-D (2003) Phylogeny of the Dictyoptera re-examined (Insecta). Entomol Abh 61:69–91
Doležel J, Bartoš J, Voglmayr H, Greihuber J (2003) Nuclear DNA content and genome size of trout and human. Cytometry A 51:127–128
Eggleton P (2001) Termites and trees: a review of recent advances in termite phylogenetics. Insectes Soc 48:187–193
Grandcolas P (1996) The phylogeny of cockroach families: a cladistic appraisal of morpho-anatomical data. Can J Zool 74:508–527
Gregory TR (2002a) Genome size and developmental complexity. Genetica 115:131–146
Gregory TR (2002b) The C-value enigma. Ph.D. Thesis, Department of Zoology, University of Guelph, Canada, pp 894
Gregory TR (2005a) Genome size evolution in animals. In: Gregory TR (ed) The evolution of the genome. Elsevier, Burlington, Massachusetts, pp 3–87
Gregory TR (2005b) Synergy between sequence and size in large scale genomics. Nat Rev Genet 6:699–708
Gregory TR (2007) Animal Genome Size Database [online]. Available from http://www.genomesize.com. [accessed 29 February 2008]
Gregory TR, Hebert PDN (1999) The modulation of DNA content: proximate causes and ultimate consequences. Genome Res 9:317–324
Greilhuber J, Doležel J, Lysák MA, Bennett MD (2005) The origin, evolution and proposed stabilization of the terms ‘genome size’ and ‘C-value’ to describe nuclear DNA contents. Ann Bot 95:255–260
Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, New York, p 755
Hardie DC, Gregory TR, Hebert PDN (2002) From pixels to picograms: a beginners’ guide to genome quantification by Feulgen image analysis densitometry. J Histochem Cytochem 50:735–749
Hayashi Y, Lo N, Miyata H, Kitade O (2007) Sex-linked genetic influence on caste determination in a termite. Science 318:985–987
Hojo M, Koshikawa S, Cornette R, Matsumoto T, Miura T (2005) Identification of soldier-specific genes in the nasute termite Nasutitermes takasagoensis (Isoptera: Termitidae). Entomol Sci 8:379–387
Hojo M, Matsumoto T, Miura T (2007) Cloning and expression of a geranylgeranyl diphosphate synthase gene—insights into the synthesis of termite defense secretion. Insect Mol Biol 16:121–131
Hughes WOH, Sumner S, Van Borm, S, Boomsma JJ (2003) Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc Nat Acad Sci USA 100:9394–9397
International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Inward D, Beccaloni G, Eggleton P (2007) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3:331–335
Johnston JS, Bennett MD, Rayburn AL, Galbraith DW, Price HJ (1999) Reference standards for determination of DNA content of plant nuclei. Am J Bot 86:609–613
Johnston JS, Ross LD, Bean L, Hughes DP, Kathirithamby J (2004) Tiny genomes and endoreduplication in Strepsiptera. Insect Mol Biol 13:581–585
Johnston JS, Yoon KS, Stbycharz JP, Pittendrigh BR, Clark JM (2007) Body lice and head lice (Anoplura: Pediculidae) have the smallest genomes of any hemimetabolous insect reported to date. J Med Entomol 44:1009–1012
Kambhampati S (2006) Termite genomics: Present knowledge and future directions. In: Proceedings of XV International Congress of IUSSI, Washington D.C., p105
Koshikawa S, Cornette R, Hojo M, Maekawa K, Matsumoto T, Miura T (2005) Screening of genes expressed in developing mandibles during soldier differentiation in the termite Hodotermopsis sjostedti. FEBS Lett 579:1365–1370
Klass KD, Meier R (2006) A phylogenetic analysis of Dictyoptera (Insecta) based on morphological characters. Entomol Abh 63:3–50
Lima-De-Faria A, Gustafsson T, Jaworska H (1973) Amplification of ribosomal DNA in Acheta II. The number of nucleotide pairs of the chromosomes and chromomers involved in amplification. Hereditas 73:119–142
Lo N, Tokuda G, Watanabe H, Rose H, Slaytor M, Maekawa K, Bandi C, Noda H (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804
Lo N, Engel MS, Cameron S, Nalepa CA, Tokuda G, Grimaldi D, Kitade O, Krishna K, Klass KD, Maekawa K, Miura T, Thompson GJ (2007) Save Isoptera: a comment on Inward et al. Biol Lett 3:562–563
Miura T, Kamikouchi A, Sawata M, Takeuchi H, Natori S, Kubo T, Matsumoto T (1999) Soldier caste-specific gene expression in the mandibular glands of Hodotermopsis japonica (Isoptera: Termopsidae). Proc Natl Acad Sci USA 96:13874–13879
Nalepa CA, Bandi C (2000) Characterizing the ancestors: paedomorphosis and termite evolution. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer, Dordrecht, The Netherlands, pp 53–75
Nalepa CA, Bell WJ (1997) Postovulation parental investment and parental care in cockroaches. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, UK, pp 26–51
Petrov DA (2001) Evolution of genome size: new approaches to an old problem. Trends Genet 17:23–28
Rasch EM, Barr HJ, Rasch RW (1971) The DNA content of sperm of Drosophila melanogaster. Chromosoma 33:1–18
Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M (eds) Termites: evolution, sociality, symbioses, ecology. Kluwer, Dordrecht, The Netherlands, pp 95–119
Scharf ME, Wu-Scharf D, Bennett GW, Pittendrigh BR (2003) Caste and development-associated gene expression in a lower termite. Genome Biol 4:R62
Scharf ME, Wu-Scharf D, Zhou X, Pittendrigh BR, Bennet GW (2005) Gene expression profiles among immature and adult reproductive castes of the termite Reticulitermes flavipes. Insect Mol Biol 14:31–44
Thorne BL (1996) Termite terminology. Sociobiology 28:253–263
Thorne BL (1997) Evolution of eusociality in termites. Annu Rev Ecol Syst 28:27–54
Westerman PK, Barton NH, Hewitt GM (1987) Differences in DNA content between two chromosomal races of the grasshopper Podisma pedestris. Heredity 58:221–228
Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, Massachusetts, p 548
Wu-Scharf D, Scharf ME, Pittendrigh BR, Bennett GW (2003) Expressed sequence tags from a polyphenic Reticulitermes flavipes cDNA library. Sociobiology 41:479–489
Zhou XG, Oi FM, Scharf ME (2006) Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc Natl Acad Sci USA 103:4499–4504
Acknowledgment
We are grateful to four anonymous referees for providing valuable suggestions. We thank N. Lo for improving the manuscript, M. Ohara and S. Kubota for instruction on flow cytometry, T.A. Evans, C. Bordereau, Y.C. Park, C. Nalepa and M. Hojo for providing samples, and K. Maekawa, A. Fujita, S. Hongo, Y. Nakamura, Y. Ishikawa and A. Ishikawa for their assistance in field sampling and advices during the study. Drosophila melanogaster Oregon R was kindly provided by T. Ide at Drosophila Stock Room of Tokyo Metropolitan University and K. Yoshida at Hokkaido University. This work was supported by KAKENHI (Nos. 18047002 and 18370007). The first and second authors were supported by JSPS Research Fellowship for Young Scientists. All research reported in this paper complies with the present laws of Japan.
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Koshikawa, S., Miyazaki, S., Cornette, R. et al. Genome size of termites (Insecta, Dictyoptera, Isoptera) and wood roaches (Insecta, Dictyoptera, Cryptocercidae). Naturwissenschaften 95, 859–867 (2008). https://doi.org/10.1007/s00114-008-0395-7
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DOI: https://doi.org/10.1007/s00114-008-0395-7