Genome size in ants: retrospect and prospect
Retrospect and Prospect
DOI:
https://doi.org/10.13128/cayologia-172Keywords:
C-value, DNA content, Genetic diversity, Genome, Evolution, PhylogenyAbstract
Genome size is very useful in studies regarding taxonomy, evolution, and reproductive biology in many animal groups, including insects. Herein, we assembled the information about genome size in ants, compiling the DNA content estimated so far, in order to evaluate the methods, the tissues and the internal standard applied to estimate the genomes size. All values were placed in a phylogenetic tree to put it in an evolutionary context and the means of the subfamilies were further compared statistically to investigate changes and trends in the variation across taxa. The compiled data resulted in 86 specimens of ants, comprising 69 different species. This number represents 0.52% of the total number of 13,369 ant species described, covering only 40 from 333 valid extant genera. The average Formicidae genome size was 0.36 pg (± 0.13). Most of the estimates were obtained through flow cytometry (83.5%), commonly using brain tissues, with Drosophila melanogaster as internal standard (76%). Differences in DNA content of ant species may be related to differences in the amount of heterochromatin and is not related with chromosome number. The evaluation of the genome size estimations currently available for ants has highlighted their scarcity. Such information would be valuable as independent data for the study of ant diversity and evolutionary biology. Further, we conclude that the standardization of the techniques used and a large–scale study on ant genome size are urgently required, given the importance of this insect group and the needs for the improvement in our knowledge on ant genome.
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References
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Bonasio R, Zhang G Ye C, Mutti NS, Fang X, Qin N, Donahue G, Yang P, Li Q, Li C, Zhang P, Huang Z, Berger SL, Reinberg D, Wang J, Liebig J (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329: 1068–1071. https://doi.org/10.1126/science.1192428
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Cardoso DC, Carvalho CR, Cristiano MP, Soares FAF, Tavares MG (2012) Estimation of nuclear genome size of the genus Mycetophylax Emery 1913: evidence of no whole–genome duplication in Neoattini. Comptes Rendus Biologies 335: 619–624. http://dx.doi.org/10.1016/j.rvi.2012.09.012
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Glancey BM, Romain MKS, Crozier RH (1976) Chromosome numbers of the red and the black imported fire ants Solenopsis invicta and S. richteri. Annals of the Entomological Society of America 69: 469–470. https://doi.org/10.1093/aesa/69.3.469
Goodisman MAD, Kovacs JL, Hunt BG (2008) Functional genetics and genomics in ants (Hymenoptera: Formicidae): The interplay of genes and social life. Myrmecological News 11: 107–117.
Gregory TR (2001) Coincidence coevolution or causation? DNA content cell size and the C–value enigma. Biological Reviews 76: 65–101. https://doi.org/10.1111/j.1469-185X.2000.tb00059.x
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Gregory TR (2005b) Genome Size Evolution in Animals in: Gregory TR (Ed) The Evolution of the Genome. Elsevier San Diego pp 3–87.
Gregory TR (2018) Animal genome size database. Available online: http://wwwgenomesizecom. [accessed 04 March 2018].
Gregory TR, Hebert PDN (1999) The modulation of DNA content: proximate causes and ultimate consequences. Genome Research 9: 317–324. https://doi.org/10.1101/gr.9.4.317
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press Cambridge.
Johnston JS, Ross LD, Beani L, Hughes DP, Kathirithamby J (2004) Tiny genomes and endoreduplication in Strepsiptera. Insect Molecular Biology 13: 581–585. https://doi.org/10.1111/j.0962-1075.2004.00514.x
Kidwell MG (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115: 49–63. https://doi.org/10.1023/A:1016072014259
Klingenberg C, Brandão CRF (2009) Revision of the fungus–growing ant genera Mycetophylax Emery and Paramycetophylax Kusnezov rev stat and description of Kalathomyrmex n gen (Formicidae: Myrmicinae: Attini). Zootaxa 2052: 1–31.
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Li J, Heinz KM (2000) Genome complexity and organization in the red imported fire ant Solenopsis invicta Buren. Genetical Research 75: 129–135
Lopes DM, Carvalho CR, Clarindo WR, Praça MM, Tavares MG (2009) Genome size estimation of three stingless bee species (Hymenoptera: Meliponinae) by flow cytometry. Apidologie 40: 517–523. https://doi.org/10.1051/apido/2009030
Lorite P, Palomeque T (2010) Karyotype evolution in ants (Hymenoptera: Formicidae) with a review of the known ant chromosome numbers. Myrmecological News 13: 89–102.
Merkel DE, Dressler LG, McGuire WL (1987) Flow cytometry cellular DNA content and prognosis in human malignancy. Journal of Clinical Oncology 5: 1690–1703. https://doi.org/10.1200/JCO.1987.5.10.1690
Moore GP (1984) The C–value paradox. BioScience 34: 425–429. https://doi.org/10.2307/1309631
Moreau CS, Bell CD (2013) Testing the museum versus cradle biological diversity hypothesis: Phylogeny diversification and ancestral biogeographic range evolution of the ants. Evolution 67: 2240–2257. https://doi.org/10.1111/evo.12105
Nygaard S, Zhang G, Schiøtt M, Li C, Wurm Y, Hu H, Zhou J, Ji L, Qiu F, Rasmussen M, Pan H, Hauser F, Krogh A, Grimmelikhuijzen CJP, Wang J, Boomsma JJ (2011) The genome of the leaf–cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome Research 21: 1339–1348. https://dx.doi.org/10.1101%2Fgr.121392.111
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Petrov DA (2001) Evolution of genome size: new approaches to an old problem. Trends in Genetics 17: 23–28. https://doi.org/10.1016/S0168-9525(00)02157-0
Price HJ, Hodnett G, Johnston S (2000) Sunflower (Helianthus annus) leaves contain compounds that reduce nuclear propidium iodide fluorescence. Annals of Botany 86: 929–934. https://doi.org/10.1006/anbo.2000.1255
R Core Team (2013) R Foundation for statistical computing. R: a language and environment for statistical computing. http://wwwR–projectorg [accessed 15 May 2017].
Sirviö A, Gadau J, Rueppell O, Lamatsch D, Boomsma JJ, Pamilo P, Page RE Jr (2006) High recombination frequency creates genotypic diversity in colonies of the leaf–cutting ant Acromyrmex echinatior. Journal of Evolutionary Biology 19: 1475–1485.
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Smith CR, Smith CD, Robertson HM, Helmkampf M, Zimin A, Yandell M, Holt C, Hu H, Abouheif E, Benton R, Cash E, Croset V, Currie CR, Elhaik E, Elsik CG, Favé M-J, Fernandes V, Gibson JD, Graur D, Gronenberg W, Grubbs KJ, Hagen DE, Viniegra ASI, Johnson BR, Johnson RM, Khila A, Kim JW, Mathis KA, Munoz-Torres MC, Murphy MC, Mustard JA, Nakamura R, Niehuis O, Nigam S, Overson RP, Placek JE, Rajakumar R, Reese JT, Suen G, Tao S, Torres CW, Tsutsui ND, Viljakainen L, Wolschin F, Gadau J (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proceedings of the National Academy of Sciences of the United States of America 108: 5667–5672. https://doi.org/10.1073/pnas.1007901108
Suen G, Teiling C, Li L, Holt C, Abouheif E, Bornberg–Bauer E, Bouffard P, Caldera EJ, Cash E, Cavanaugh A, Denas O, Elhaik E, Favé MJ, Gadau J, Gibson JD, Graur D, Grubbs KJ, Hagen DE, Harkins TT, Helmkampf M, Hu H, Johnson BR, Kim J, Marsh SE, Moeller JA, Muñoz–Torres MC, Murphy MC, Naughton MC, Nigam S, Overson R, Rajakumar R, Reese JT, Scott JJ, Smith CR, Tao S, Tsutsui ND, Viljakainen L, Wissler L, Yandell MD, Zimmer F, Taylor J, Slater SC, Clifton SW, Warren WC, Elsik CG, Smith CD, Weinstock GM, Gerardo NM, Currie CR (2011) The genome sequence of the leaf–cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genetics 7: e1002007. https://doi.org/10.1371/journal.pgen.1002007
Tavares MG, Carvalho CR, Soares FAF (2010) Genome size variation in Melipona species (Hymenoptera: Apidae) and sub–grouping by their DNA content. Apidologie 41: 636–642. https://doi.org/10.1051/apido/20010023
Tavares MG, Carvalho CR, Soares FAF, Campos LAO (2012) Genome size diversity in stingless bees (Hymenoptera: Apidae, Meliponini). Apidologie 43: 731–736. https://doi.org/10.1007/s13592-012-0145-x
Tavares MG, Lopes DM, Campos LAO (2017) An overview of cytogenetics of the tribe Meliponini (Hymenoptera: Apidae). Genetica 145 241–258. https://doi.org/10.1007/s10709-017-9961-2
Torresan F, Zanella L, Mattarozzi A, Quiroga A, Bacchini P, Bertoni F, Gandolfi L (1994) DNA analysis with flow cytometry and image cytometry in colorectal polyps. Surgical Endoscopy 8: 1412–1416.
Tsutsui ND, Suarez AV, Spagna JC, Johnston JS (2008) The evolution of genome size in ants. BMC Evolutionary Biology 8: 64. https://doi.org/10.1186/1471-2148-8-64
Vieira C, Nardon C, Arpin C, Lepetit D, Biémont C (2002) Evolution of genome size in Drosophila Is the invader’s genome being invaded by transposable elements? Molecular Biology and Evolution 19: 1154–1161. https://doi.org/10.1093/oxfordjournals.molbev.a004173
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Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2007) Molecular biology of the cell fifth ed. Garland Science New York.
Alfsnes K, Leinaas HP, Hessen DO (2017) Genome size in arthropods, different roles of phylogeny habitat and life history in insects and crustaceans. Ecology and Evolution 7: 5939–5947. https://doi.org/10.1002/ece3.3163
Ardila–Garcia AM, Gregory TR (2009) An exploration of genome size diversity in dragonflies and damselflies (Insecta: Odonata). Journal of Zoology 278: 163–173. https://doi.org/10.1111/j.1469-7998.2009.00557.x
Ardila–Garcia AM, Umphrey GJ, Gregory TR (2010) An expansion of the genome size dataset for the insect order Hymenoptera with a first test of parasitism and eusociality as possible constraints. Insect Molecular Biology 19: 337–346. https://doi.org/10.1111/j.1365-2583.2010.00992.x
Basiji DA, Ortyn WE, Liang L, Venkatachalam V, Morrissey P (2007) Cellular image analysis and imaging by flow cytometry. Clinics in Laboratory Medicine 27: 653–70. https://doi.org/10.1016/j.cll.2007.05.008
Bolton, B. 2018. An online catalog of the ants of the world. Available from http://antcat.org. [accessed 04 March 2018].
Bonasio R, Zhang G Ye C, Mutti NS, Fang X, Qin N, Donahue G, Yang P, Li Q, Li C, Zhang P, Huang Z, Berger SL, Reinberg D, Wang J, Liebig J (2010) Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329: 1068–1071. https://doi.org/10.1126/science.1192428
Brandão CRF (1999) Família Formicidae in: Brandão CRF, Cancello EM (Eds) Invertebrados terrestres. ed. Biodiversidade do Estado de São Paulo: síntese do conhecimento ao final do século XX. (Joly CA Bicudo CEM (orgs)) FAPESP São Paulo pp 215–223.
Cardoso DC, Carvalho CR, Cristiano MP, Soares FAF, Tavares MG (2012) Estimation of nuclear genome size of the genus Mycetophylax Emery 1913: evidence of no whole–genome duplication in Neoattini. Comptes Rendus Biologies 335: 619–624. http://dx.doi.org/10.1016/j.rvi.2012.09.012
Crawley MJ (2013) The R Book second ed. John Wiley & Sons Ltd. London.
Doležel J, Bartoš J (2005) Plant DNA flow cytometry and estimation of nuclear genome size. Annals of Botany 95: 99–110. https://doi.org/10.1093/aob/mci005
Doležel J, Bartoš J, Voglmayr H, Greilhuber J (2003) Nuclear DNA content and genome size of trout and human. Cytometry. Part A 51: 127–128. https://doi.org/10.1002/cyto.a.10013
Doležel J, Greilhuber J (2010) Nuclear genome size: are we getting closer? Cytometry. Part A 77A: 635–642. https://doi.org/10.1002/cyto.a.20915
Doležel J, Greilhuber J, Suda J (2007) Estimation of nuclear DNA content in plants using flow cytometry. Nature Protocols 2 2233–2244. https://doi.org/10.1038/nprot.2007.310
Dufresne F, Jeffery N (2011) A guided tour of large genome size in animals: what we know and where we are heading. Chromosome Research 19: 925–938. https://doi.org/10.1007/s10577-011-9248-x
Eddy SR (2012) The C–value paradox junk DNA and ENCODE. Current Biology 22: 898–899. https://doi.org/10.1016/j.cub.2012.10.002
Françoso ML, Brandão CRF (1993) Classificação superior dos Formicidae. Biotemas 6: 121–132. https://doi.org/10.5007/%25x
Glancey BM, Romain MKS, Crozier RH (1976) Chromosome numbers of the red and the black imported fire ants Solenopsis invicta and S. richteri. Annals of the Entomological Society of America 69: 469–470. https://doi.org/10.1093/aesa/69.3.469
Goodisman MAD, Kovacs JL, Hunt BG (2008) Functional genetics and genomics in ants (Hymenoptera: Formicidae): The interplay of genes and social life. Myrmecological News 11: 107–117.
Gregory TR (2001) Coincidence coevolution or causation? DNA content cell size and the C–value enigma. Biological Reviews 76: 65–101. https://doi.org/10.1111/j.1469-185X.2000.tb00059.x
Gregory TR (2005a) The C–value enigma in plants and animals: a review of parallels and an appeal for partnership. Annals of Botany 95: 133–146. https://dx.doi.org/10.1093%2Faob%2Fmci009
Gregory TR (2005b) Genome Size Evolution in Animals in: Gregory TR (Ed) The Evolution of the Genome. Elsevier San Diego pp 3–87.
Gregory TR (2018) Animal genome size database. Available online: http://wwwgenomesizecom. [accessed 04 March 2018].
Gregory TR, Hebert PDN (1999) The modulation of DNA content: proximate causes and ultimate consequences. Genome Research 9: 317–324. https://doi.org/10.1101/gr.9.4.317
Hölldobler B, Wilson EO (1990) The ants. Harvard University Press Cambridge.
Johnston JS, Ross LD, Beani L, Hughes DP, Kathirithamby J (2004) Tiny genomes and endoreduplication in Strepsiptera. Insect Molecular Biology 13: 581–585. https://doi.org/10.1111/j.0962-1075.2004.00514.x
Kidwell MG (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115: 49–63. https://doi.org/10.1023/A:1016072014259
Klingenberg C, Brandão CRF (2009) Revision of the fungus–growing ant genera Mycetophylax Emery and Paramycetophylax Kusnezov rev stat and description of Kalathomyrmex n gen (Formicidae: Myrmicinae: Attini). Zootaxa 2052: 1–31.
Klug WS, Cummings MR, Spencer CA, Palladino MA (2014) Concepts of genetics eleventh. Ed. Pearson. New Jersey
Li J, Heinz KM (2000) Genome complexity and organization in the red imported fire ant Solenopsis invicta Buren. Genetical Research 75: 129–135
Lopes DM, Carvalho CR, Clarindo WR, Praça MM, Tavares MG (2009) Genome size estimation of three stingless bee species (Hymenoptera: Meliponinae) by flow cytometry. Apidologie 40: 517–523. https://doi.org/10.1051/apido/2009030
Lorite P, Palomeque T (2010) Karyotype evolution in ants (Hymenoptera: Formicidae) with a review of the known ant chromosome numbers. Myrmecological News 13: 89–102.
Merkel DE, Dressler LG, McGuire WL (1987) Flow cytometry cellular DNA content and prognosis in human malignancy. Journal of Clinical Oncology 5: 1690–1703. https://doi.org/10.1200/JCO.1987.5.10.1690
Moore GP (1984) The C–value paradox. BioScience 34: 425–429. https://doi.org/10.2307/1309631
Moreau CS, Bell CD (2013) Testing the museum versus cradle biological diversity hypothesis: Phylogeny diversification and ancestral biogeographic range evolution of the ants. Evolution 67: 2240–2257. https://doi.org/10.1111/evo.12105
Nygaard S, Zhang G, Schiøtt M, Li C, Wurm Y, Hu H, Zhou J, Ji L, Qiu F, Rasmussen M, Pan H, Hauser F, Krogh A, Grimmelikhuijzen CJP, Wang J, Boomsma JJ (2011) The genome of the leaf–cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome Research 21: 1339–1348. https://dx.doi.org/10.1101%2Fgr.121392.111
Oliver MJ, Petrov D, Ackerly D, Falkowski P, Schofield OM (2007) The mode and tempo of genome size evolution in eukaryotes. Genome Research 17: 594–601. https://dx.doi.org/10.1101%2Fgr.6096207
Pellicer J, Hidalgo O, Dodsworth S, Leitch IJ (2018) Genome Size Diversity and Its Impact on the Evolution of Land Plants. Genes 9: 88. https://doi.org/10.3390/genes9020088
Petrov DA (2001) Evolution of genome size: new approaches to an old problem. Trends in Genetics 17: 23–28. https://doi.org/10.1016/S0168-9525(00)02157-0
Price HJ, Hodnett G, Johnston S (2000) Sunflower (Helianthus annus) leaves contain compounds that reduce nuclear propidium iodide fluorescence. Annals of Botany 86: 929–934. https://doi.org/10.1006/anbo.2000.1255
R Core Team (2013) R Foundation for statistical computing. R: a language and environment for statistical computing. http://wwwR–projectorg [accessed 15 May 2017].
Sirviö A, Gadau J, Rueppell O, Lamatsch D, Boomsma JJ, Pamilo P, Page RE Jr (2006) High recombination frequency creates genotypic diversity in colonies of the leaf–cutting ant Acromyrmex echinatior. Journal of Evolutionary Biology 19: 1475–1485.
Smith CD, Zimin A, Holt C, Abouheif E, Benton R, Cash E, Croset V, Currie CR, Elhaik E, Elsik CG, Fave M-J, Fernandes V, Gadau J, Gibson JD, Graur D, Grubbs KJ, Hagen DE, Helmkampf M, Holley JA, Hu H, Viniegra ASI, Johnson BR, Johnson RM, Khila A, Kim JW, Laird J, Mathis KA, Moeller JA, Muñoz-Torres MC, Murphy MC, Nakamura R, Nigam S, Overson RP, Placek JE, Rajakumar R, Reese JT, Robertson HM, Smith CR, Suarez AV, Suen G, Suhr EL, Tao S, Torres CW, Wilgenburg EV, Viljakainen L, Walden KKO, Wild AL, Yandell M, Yorke JA Tsutsui ND (2011) Draft genome of the globally widespread and invasive Argentine ant (Linepithema humile). Proceedings of the National Academy of Sciences of the United States of America 108: 5673–5678. https://doi.org/10.1073/pnas.1008617108
Smith CR, Smith CD, Robertson HM, Helmkampf M, Zimin A, Yandell M, Holt C, Hu H, Abouheif E, Benton R, Cash E, Croset V, Currie CR, Elhaik E, Elsik CG, Favé M-J, Fernandes V, Gibson JD, Graur D, Gronenberg W, Grubbs KJ, Hagen DE, Viniegra ASI, Johnson BR, Johnson RM, Khila A, Kim JW, Mathis KA, Munoz-Torres MC, Murphy MC, Mustard JA, Nakamura R, Niehuis O, Nigam S, Overson RP, Placek JE, Rajakumar R, Reese JT, Suen G, Tao S, Torres CW, Tsutsui ND, Viljakainen L, Wolschin F, Gadau J (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proceedings of the National Academy of Sciences of the United States of America 108: 5667–5672. https://doi.org/10.1073/pnas.1007901108
Suen G, Teiling C, Li L, Holt C, Abouheif E, Bornberg–Bauer E, Bouffard P, Caldera EJ, Cash E, Cavanaugh A, Denas O, Elhaik E, Favé MJ, Gadau J, Gibson JD, Graur D, Grubbs KJ, Hagen DE, Harkins TT, Helmkampf M, Hu H, Johnson BR, Kim J, Marsh SE, Moeller JA, Muñoz–Torres MC, Murphy MC, Naughton MC, Nigam S, Overson R, Rajakumar R, Reese JT, Scott JJ, Smith CR, Tao S, Tsutsui ND, Viljakainen L, Wissler L, Yandell MD, Zimmer F, Taylor J, Slater SC, Clifton SW, Warren WC, Elsik CG, Smith CD, Weinstock GM, Gerardo NM, Currie CR (2011) The genome sequence of the leaf–cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genetics 7: e1002007. https://doi.org/10.1371/journal.pgen.1002007
Tavares MG, Carvalho CR, Soares FAF (2010) Genome size variation in Melipona species (Hymenoptera: Apidae) and sub–grouping by their DNA content. Apidologie 41: 636–642. https://doi.org/10.1051/apido/20010023
Tavares MG, Carvalho CR, Soares FAF, Campos LAO (2012) Genome size diversity in stingless bees (Hymenoptera: Apidae, Meliponini). Apidologie 43: 731–736. https://doi.org/10.1007/s13592-012-0145-x
Tavares MG, Lopes DM, Campos LAO (2017) An overview of cytogenetics of the tribe Meliponini (Hymenoptera: Apidae). Genetica 145 241–258. https://doi.org/10.1007/s10709-017-9961-2
Torresan F, Zanella L, Mattarozzi A, Quiroga A, Bacchini P, Bertoni F, Gandolfi L (1994) DNA analysis with flow cytometry and image cytometry in colorectal polyps. Surgical Endoscopy 8: 1412–1416.
Tsutsui ND, Suarez AV, Spagna JC, Johnston JS (2008) The evolution of genome size in ants. BMC Evolutionary Biology 8: 64. https://doi.org/10.1186/1471-2148-8-64
Vieira C, Nardon C, Arpin C, Lepetit D, Biémont C (2002) Evolution of genome size in Drosophila Is the invader’s genome being invaded by transposable elements? Molecular Biology and Evolution 19: 1154–1161. https://doi.org/10.1093/oxfordjournals.molbev.a004173
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2019-12-23
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Moura, M. N., Cardoso, D. C., Baldez, B. C. L., & Cristiano, M. P. (2019). Genome size in ants: retrospect and prospect: Retrospect and Prospect. Caryologia, 72(4), 29–39. https://doi.org/10.13128/cayologia-172
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