Abstract
Avian genomes are of interest because the rapid metabolic rate associated with powered flight requires small cells which constrain genome size. Consequently, flying birds tend to have small genomes relative to other vertebrates such as mammals. It thus stands to reason that flying birds should have smaller genomes than ground-dwelling birds with lower metabolic rates. Small genomes could be condensed but uncompromised in a number of ways, including smaller intergenic intervals, shorter introns, and/or a reduced transposable element (TE) complement. We evaluated genome size in light of the orthologous TE complement among 41 flying (FY) and seven ground-dwelling (GD) bird species to determine if a preponderance of deletions in orthologous TEs might explain the compact genomes of flying birds with high metabolic rates. We measured, across multiple loci in all 48 species, the lengths of 50 contemporary orthologous chicken repeat 1 (CR1, a non-LTR retrotransposon) copies relative to inferred ancestral CR1 sequences. We found genome sizes in GD birds were not different than those in FY birds, but the mean lengths of orthologous CR1 loci were significantly shorter in FY birds than in GD birds. Moreover, we observed a negative correlation between basal metabolic rate and length of orthologous CR1 loci. Finally, we observed positive correlations between body mass and both genome sizes as well as length of orthologous CR1 loci, which we expected given that body mass correlates negatively with metabolic rates. Our results support the contention that metabolism helps shape the avian TE complement and thus indirectly contributes to the compact genomes of birds.
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References
Aguilar, V., & Fajas, L. (2010). Cycling through metabolism. EMBO Molecular Medicine, 2(9), 338–348.
Andrews, C. B., Mackenzie, S. A. & Gregory, T. R. (2009). Genome size and wing parameters in passerine birds. Proceedings Royal S ociety B-Biology, 276(1654), 55–61.
Bartosch-Härlid, A. et al. (2003). Life history and the male mutation bias. Evolution, 57(10), 2398. http://www.bioone.org/perlserv/?request=get-abstract&doi=10.1554/03-036.
Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution; International Journal Of Organic Evolution, 57(4), 717–745.
Cavalier-Smith, T. (1985). The evolution of genome size in birds.
Drost, J. B. & Lee, W. R. (1995). Biological basis of germline mutation: comparisons of spontaneous germline mutation rates among drosophila, mouse, and human. Environmental and Molecular Mutagenesis, 25(suppl. 2), 48–64.
Dunning, J. B. (2007). CRC Handbook of avian body masses. 2nd ed., Boca Raton: CRC Press.
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–7. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=390337&tool=pmcentrez&rendertype=abstract. Accessed 11 July 2014.
Elliott, T. A. & Gregory, T. R. (2015). What’s in a genome? The C-value enigma and the evolution of eukaryotic genome content. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 370(1678).
Feduccia, A. (1999). The evolution of flightlessness. In The origin and evolution of birds. p. 466.
Gregory, T. R. (2002). A bird’s-eye view of the C-value enigma: genome size, cell size, and metabolic rate in the class Aves. Evolution, 56(1), 121–130.
Gregory, T. R. (2003). Is small indel bias a determinant of genome size? Trends in Genetics, 19(9), 485–488.
Gregory, T. R. (2005). Genome size evolution in animals. In London: Elsevier Academic Press. pp. 4–87.
Heiden Vander, M. G. et al. (2009). Understanding the Warburg Effect: Cell Proliferation. Science, 324, 1029–1034.
Hughes, A. L. (1999). Adaptive evolution of genes and genomes. Oxford: Oxford University Press.
Hughes, A. L., & Hughes, M. K. (1995). Small genomes for better flyers. Nature, 377(5), 391.
Jarvis, E. D. (2014). Whole-genome analyses resolve early branches in the tree of life of modern birds. Science, 346(6215), 1320–1331.
Jurka, J. et al. (2005). Repbase Update, a database of eukaryotic repetitive elements. Cytogenetic and Genome Research, 110(1–4), 462–7.
Karolchik, D. et al. (2004). The UCSC Table Browser data retrieval tool. Nucleic Acids Research, 32(suppl 1), D493–D496. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=308837&tool=pmcentrez&rendertype=abstract.
Kozlowski, J. (2010). Cell size is positively correlated between different tissues in passerine birds and amphibians, but not necessarily in mammals Cell size is positively correlated between different tissues in passerine birds and amphibians, but not necessarily in mammals. Biology Letters, 6(6), 792–796.
Kozłowski, J., Konarzewski, M. & Gawelczyk, A. T. (2003). Cell size as a link between noncoding DNA and metabolic rate scaling. Proceedings of the National Academy of Sciences of the United States of America, 100(24), 14080–14085.
Kvikstad, E. M., Chiaromonte, F., & Makova, K. D. (2009). Ride the wavelet: A multiscale analysis of genomic contexts flanking small insertions and deletions. Genome Research, 19(814), 1153–1164.
Kvikstad, E. M. et al. (2007). A macaque’s-eye view of human insertions and deletions: differences in mechanisms. PLoS Computational Biology, 3(9), 1772–82. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1976337&tool=pmcentrez&rendertype=abstract. Accessed 24 Oct 2015.
Li, R. et al. (2010). The sequence and de novo assembly of the giant panda genome. Nature, 463(7279), 311–7. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3951497&tool=pmcentrez&rendertype=abstract. Accessed 16 July 2014.
Li, X., & Waterman, M. S. (2003). Estimating the Repeat Structure and Length of DNA Sequences Using l-Tuples. Genome Research, 13, 1916–1922.
Liu, B. et al. (2013). Estimation of genomic characteristics by analyzing k- mer frequency in de novo genome projects Keywords. arXiv, (1308.2012). http://arxiv.org/abs/1308.2012.
Lovsin, N., Gubensek, F., & Kordis, D. (2001). Evolutionary Dynamics in a Novel L2 Clade of Non-LTR Retrotransposons in Deuterostomia. Molecular Biology and Evolution, 18(12), 2213–2224.
Luan, D. D. et al. (1993). Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: A mechanism for non-LTR retrotransposition. Cell, 72(4), 595–605. http://linkinghub.elsevier.com/retrieve/pii/0092867493900785.
Lynch, M. & Conery, J. S. (2003). The origins of genome complexity. Science, 302(5649), 1401–4.
Macas, J. et al. (2015). In Depth Characterization of Repetitive DNA in 23 Plant Genomes Reveals Sources of Genome Size Variation in the Legume Tribe Fabeae. PLoS One, 10(11), e0143424. http://dx.plos.org/10.1371/journal.pone.0143424.
Makarieva, A. M. (2008). Mean mass-specific metabolic rates are strikingly similar across life’s major domains: Evidence for life’s metabolic optimum. Proceedings of the National Academy of Sciences of the United States of America, 105(44), 16994–16999.
Makova, K. D., Yang, S. & Chiaromonte, F. (2004). Insertions and deletions are male biased too: a whole-genome analysis in rodents. Genome Research, 14(4), 567–73. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=383300&tool=pmcentrez&rendertype=abstract.
Marçais, G. & Kingsford, C. (2011). A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics (Oxford, England), 27(6), 764–70. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3051319&tool=pmcentrez&rendertype=abstract. Accessed 10 July 2014.
Martin, A. P. & Palumbi, S. R. (1993). Body size, metabolic rate, generation time, and the molecular clock. Proceedings of the National Academy of Sciences of the United States of America, 90, 4087–4091.
McNab, B. K. & Ellis, H. I. (2006). Flightless rails endemic to islands have lower energy expenditures and clutch sizes than flighted rails on islands and continents. Comparative Biochemistry & Physiology A, 145(3), 295–311.
McNab, K. (1994). Energy conservation and the evolution of flightlessness in birds. The American Naturalist, 144(4), 628–642.
Miller, J. R., Koren, S. & Sutton, G. (2010). Assembly algorithms for next-generation sequencing data. Genomics, 95(6), 315–27. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2874646&tool=pmcentrez&rendertype=abstract. Accessed 10 July 2014.
Organ, C. L., & Edwards, S. V. (2011). Major Events in Avian Genome Evolution. In Living dinosaurs: the evolutionary history of modern birds. pp. 343–355.
Organ, C. L. et al. (2007). Origin of avian genome size and structure in non-avian dinosaurs. Nature, 446(7132), 180–4.
Organ, C. L. & Shedlock, A. M. (2009). Palaeogenomics of pterosaurs and the evolution of small genome size in flying vertebrates. Biology Letters, 5(1), 47–50. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2657748&tool=pmcentrez&rendertype=abstract. Accessed 25 May 2014.
Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401(6756), 877–884.
Petrov, D. A. & Hartl, D. L. (1998). High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Molecular Biology and Evolution, 15(3), 293–302. http://mbe.oxfordjournals.org/cgi/doi/10.1093/oxfordjournals.molbev.a025926.
Piersma, T. (1988). Breast muscle atrophy and constraints on foraging during the flightless period of wing molting great crested grebes. Ardea, 76, 82–95.
Quinlan, A. R. & Hall, I. M. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics (Oxford, England), 26(6), 841–2. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2832824&tool=pmcentrez&rendertype=abstract. Accessed 9 July 2014.
R Core Team. (2016). R: A language and environment for statistical computing. http://www.r-project.org.
Rand, D. M. (1993). Endotherms, ectotherms, and mitochondrial genome-size variation. Journal of Molecular Evolution, 37(3), 281–295.
Revell, L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217–223.
Revell, L. J. (2010). Phylogenetic signal and linear regression on species data. Methods in Ecology and Evolution, 1(4), 319–329. http://www.<Go\nto\nISI>000288914700001.
Reynolds, A. P. S., & Lee, R. M. III (1996). Analysis of avian energetics: passerines and nonpasserines do not differ. The American Naturalist, 147(5), 735–759.
Rice, P., Longden, I., & Bleasby, A. (2000). EMBOSS: The European Molecular Biology Open Software Suite. Trends in Genetics: TIG, 16(6), 2–3.
Shen, Y. Y. (2009). Relaxation of selective constraints on avian mitochondrial DNA following the degeneration of flight ability. Genome Research, 19(10), 1760–1765.
Smith, J. D. L., Bickham, J. W. & Gregory, T. R. (2013). Patterns of genome size diversity in bats (order Chiroptera). Genome, 56(8), 457–72.
Smith, J. J. et al. (2009). Genic regions of a large salamander genome contain long introns and novel genes. BMC Genomics, 10, 19. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2633012&tool=pmcentrez&rendertype=abstract. Accessed 25 Oct 2015.
Suh, A. et al. (2011). Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nature Communications, 2, 443. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3265382&tool=pmcentrez&rendertype=abstract. Accessed 20 March 2015.
Sun, C., López Arriaza, J. R. & Mueller, R. L. (2012). Slow DNA loss in the gigantic genomes of salamanders. Genome Biology and Evolution, 4(12), 1340–8. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3542557&tool=pmcentrez&rendertype=abstract. Accessed 20 Feb 2015.
Sundström, H., Webster, M. T., & Ellegren, H. (2003). Is the rate of insertion and deletion mutation male biased?: Molecular evolutionary analysis of avian and primate sex chromosome sequences. Genetics, 164(1), 259–268.
Szarski, H. (1976). Cell size and nuclear DNA content in vertebrates. International Review of Cytology, 44, 93–113.
Szarski, H. (1983). Cell size and the concept of wasteful and frugal evolutionary strategies. Journal of Theoretical Biology, 105(2), 201–209. http://linkinghub.elsevier.com/retrieve/pii/S0022519383800022.
Tiersch, T. R. & Wachtel, S. S. (1991). On the evolution of genome size of birds. The Journal of heredity, 82(5), 363–8.
Vinogradov, A. E. & Anatskaya, O. V. (2006). Genome size and metabolic intensity in tetrapods: a tale of two lines. Proceedings of the Royal Society B: Biological Sciences, 273(1582), 27–32. http://rspb.royalsocietypublishing.org/cgi/doi/10.1098/rspb.2005.3266 Accessed 15 Oct 2015.
Vu, G. T. H. et al. (2015). Comparative Genome Analysis Reveals Divergent Genome Size Evolution in a Carnivorous Plant Genus. The Plant Genome, 8(3). https://dl.sciencesocieties.org/publications/tpg/abstracts/0/0/plantgenome2015.04.0021. Accessed 23 Oct 2015.
Wright, N. A. (2015). The effects of ecology and evolution on avian flight morphology.
Wright, N. A., Gregory, T. R. & Witt, C. C. (2014). Metabolic “engines” of flight drive genome size reduction in birds. Proceedings of the Royal Society: Biological Sciences, 281, 20132780.
Zhang, G. et al. (2014). Comparative genomics reveals insights into avian genome evolution and adaptation. Science, 346(6215), 1311–1320. http://www.sciencemag.org/content/346/6215/1311.abstract.
Zhang, Q. & Edwards, S. V (2012). The evolution of intron size in amniotes: a role for powered flight? Genome Biology and Evolution, 4(10), 1033–43. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3490418&tool=pmcentrez&rendertype=abstract. Accessed 23 May 2014.
Zuccolo, A. et al. (2007). Transposable element distribution, abundance and role in genome size variation in the genus Oryza. BMC Evolutionary Biology, 7, 152. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2041954&tool=pmcentrez&rendertype=abstract. Accessed 25 Oct 2015.
Acknowledgements
We thank Purdue’s Department of Forestry and Natural Resources and the China Scholarship Council for funding Y. J and Purdue’s Office of the Provost for funding J.A.D through the University Faculty Scholar program. We thank M. Sundaram for statistical suggestions and members of DeWoody Lab for constructive criticisms on an earlier version of the manuscript.
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Ji, Y., DeWoody, J.A. Relationships Among Powered Flight, Metabolic Rate, Body Mass, Genome Size, and the Retrotransposon Complement of Volant Birds. Evol Biol 44, 261–272 (2017). https://doi.org/10.1007/s11692-016-9405-4
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DOI: https://doi.org/10.1007/s11692-016-9405-4