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Evolutionary Biology

, Volume 44, Issue 2, pp 190–205 | Cite as

Junk DNA Contribution to Evolutionary Capacitance Can Drive Species Dynamics

  • Carlos Díaz-CastilloEmail author
Synthesis Paper

Abstract

Junk DNA is still an enigmatic concept. Although junk DNA composition, abundance, and functionality are still contentious, its contribution to biological evolution is less questionable. Recently, I proposed that sexually restricted chromosomes such as Y and W, highly enriched in junk DNA elements, act as genomic tuning knobs indirectly causing a genome-wide increase in gene expression heterogeneity that boosts heterogametic individuals ability to endure environmental challenges and evolutionary capacitance, i.e., the store of genetic variation with no phenotypic effect. Sexually restricted chromosomes-based evolutionary capacitance might importantly contribute to metazoan sexual dimorphisms for dispersal and sex-biased gene expression dynamics. In this Synthesis, I hypothesize that large differences between species in the overall amount of junk DNA within their genomes also promote differences in junk DNA-based evolutionary capacitance that might be reflected in differences for dispersal and genetic diversification. I hypothesize that populations for species with junk DNA-impoverished genomes would show an enhanced ability to genetically diversify leading to a faster speciation rate even in the absence of geographic isolation when compared with populations for species with junk DNA-enriched genomes. To support junk DNA variation-based evolutionary capacitance effect on species genetic diversification, I analyzed the covariation of genome size as proxy for the overall amount of junk DNA in the genome and several genetic diversification measures obtained from interspecific crosses for the Drosophilidae family. The potential effect of junk DNA variation-based evolutionary capacitance for other elements of species dynamics such as extinction or the participation in grouped ecological structures is also briefly discussed.

Keywords

Junk DNA Genomic tuning knobs Evolutionary capacitance Heterochromatin Gene expression heterogeneity Speciation Dispersal Extinction 

Notes

Acknowledgements

The author wants to express his deepest gratitude to Raquel Chamorro-García for valuable comments during the preparation of this article and her constant support.

Compliance with Ethical Standards

Conflict of interest

The author declares that he has no conflict of interest.

Supplementary material

11692_2016_9404_MOESM1_ESM.xlsx (31 kb)
Supplementary material 1 (XLSX 30 KB)
11692_2016_9404_MOESM2_ESM.xlsx (29 kb)
Supplementary material 2 (XLSX 29 KB)

References

  1. Allaby, M. (2003). A dictionary of zoology. New York: Oxford University Press.Google Scholar
  2. Assis, R., Zhou, Q., & Bachtrog, D. (2012). Sex-biased transcriptome evolution in Drosophila. Genome Biology and Evolution, 4(11), 1189–1200. doi: 10.1093/gbe/evs093.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bächli, G. (2015). TaxoDros v1.04. The database on Taxonomy of Drosophilidae.http://www.taxodros.uzh.ch.http://www.taxodros.uzh.ch.
  4. Bachtrog, D. (2013). Y-chromosome evolution: Emerging insights into processes of Y-chromosome degeneration. Nature Reviews Genetics, 14(2), 113–124. doi: 10.1038/nrg3366.PubMedPubMedCentralCrossRefGoogle Scholar
  5. Banaszynski, L. A., Allis, C. D., & Lewis, P. W. (2010). Histone variants in metazoan development. Developmental Cell, 19(5), 662–674. doi: 10.1016/j.devcel.2010.10.014.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Baroux, C., Autran, D., Gillmor, C. S., Grimanelli, D., & Grossniklaus, U. (2008). The maternal to zygotic transition in animals and plants. Cold Spring Harbor Symposia on Quantitative Biology, 73(0), 89–100. doi: 10.1101/sqb.2008.73.053.PubMedCrossRefGoogle Scholar
  7. Barron, A. B. (2015). Death of the bee hive: Understanding the failure of an insect society. Current Opinion in Insect Science, 10, 45–50. doi: 10.1016/j.cois.2015.04.004.CrossRefGoogle Scholar
  8. Barron, M. G., Fiston-Lavier, A. S., Petrov, D. A., & Gonzalez, J. (2014). Population genomics of transposable elements in Drosophila. Annual Review of Genetics, 48(1), 561–581. doi: 10.1146/annurev-genet-120213-092359.PubMedCrossRefGoogle Scholar
  9. Bennett, M. D. (1976). DNA amount, latitude, and crop plant distribution. Environmental and Experimental Botany, 16(2–3), 93–108. doi: 10.1016/0098-8472(76)90001-0.CrossRefGoogle Scholar
  10. Berloco, M., Palumbo, G., Piacentini, L., Pimpinelli, S., & Fanti, L. (2014). Position effect variegation and viability are both sensitive to dosage of constitutive heterochromatin in Drosophila. G3 (Bethesda), 4(9), 1709–1716, doi: 10.1534/g3.114.013045.CrossRefGoogle Scholar
  11. Biamonti, G., & Vourc’h, C. (2010). Nuclear stress bodies. Cold Spring Harbor Perspectives in Biology, 2(6), a000695. doi: 10.1101/cshperspect.a000695.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Biemont, C. (2010). A brief history of the status of transposable elements: From junk DNA to major players in evolution. Genetics, 186(4), 1085–1093. doi: 10.1534/genetics.110.124180.PubMedPubMedCentralCrossRefGoogle Scholar
  13. Blaxter, M., & Koutsovoulos, G. (2015). The evolution of parasitism in Nematoda. Parasitology, 142(Suppl 1), S26–S39, doi: 10.1017/S0031182014000791.PubMedCrossRefGoogle Scholar
  14. Bohne, A., Brunet, F., Galiana-Arnoux, D., Schultheis, C., & Volff, J. N. (2008). Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Research, 16(1), 203–215. doi: 10.1007/s10577-007-1202-6.PubMedCrossRefGoogle Scholar
  15. Bosco, G., Campbell, P., Leiva-Neto, J. T., & Markow, T. A. (2007). Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics, 177(3), 1277–1290. doi: 10.1534/genetics.107.075069.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Carswell, C. (2015). Climate change. Bumblebees aren’t keeping up with a warming planet. Science, 349(6244), 126–127. doi: 10.1126/science.349.6244.126.PubMedCrossRefGoogle Scholar
  17. Drosophila 12 Genomes Consortium, Clark, A. G., Eisen, M. B., Smith, D. R., Bergman, C. M., Oliver, B., et al. (2007). Evolution of genes and genomes on the Drosophila phylogeny. Nature, 450(7167), 203–218. doi: 10.1038/nature06341.CrossRefGoogle Scholar
  18. Clobert, J., Baguette, M., Benton, T. G., Bullock, J. M., & Ducatez, S. (2012). Dispersal ecology and evolution. Oxford: Oxford University Press.CrossRefGoogle Scholar
  19. Cohen, S., Agmon, N., Yacobi, K., Mislovati, M., & Segal, D. (2005). Evidence for rolling circle replication of tandem genes in Drosophila. Nucleic Acids Research, 33(14), 4519–4526. doi: 10.1093/nar/gki764.PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cohen, S., & Segal, D. (2009). Extrachromosomal circular DNA in eukaryotes: possible involvement in the plasticity of tandem repeats. Cytogenetic and Genome Research, 124(3–4), 327–338. doi: 10.1159/000218136.PubMedCrossRefGoogle Scholar
  21. Coyne, J. A., & Orr, H. A. (1989). Patterns of speciation in Drosophila. Evolution, 43(2), 362. doi: 10.2307/2409213.CrossRefGoogle Scholar
  22. Coyne, J. A., & Orr, H. A. (1997). “Patterns of speciation in Drosophila” revisited. Evolution, 51(1), 295. doi: 10.2307/2410984.CrossRefGoogle Scholar
  23. David, J. R., Lemeunier, F., Tsacas, L., & Yassin, A. (2007). The historical discovery of the nine species in the Drosophila melanogaster species subgroup. Genetics, 177(4), 1969–1973. doi: 10.1534/genetics.104.84756.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Diaz-Castillo, C. (2013). Females and males contribute in opposite ways to the evolution of gene order in Drosophila. PLoS One, 8(5), e64491. doi: 10.1371/journal.pone.0064491.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Diaz-Castillo, C. (2015). Evidence for a sexual dimorphism in gene expression noise in metazoan species. PeerJ, 3(Suppl 1), e750. doi: 10.7717/peerj.750.PubMedPubMedCentralCrossRefGoogle Scholar
  26. Diaz-Castillo, C., & Ranz, J. M. (2012). Nuclear chromosome dynamics in the Drosophila male germ line contribute to the nonrandom genomic distribution of retrogenes. Molecular Biology and Evolution, 29(9), 2105–2108. doi: 10.1093/molbev/mss096.PubMedCrossRefGoogle Scholar
  27. Diez, C. M., Gaut, B. S., Meca, E., Scheinvar, E., Montes-Hernandez, S., Eguiarte, L. E., et al. (2013). Genome size variation in wild and cultivated maize along altitudinal gradients. The New Phytologist, 199(1), 264–276. doi: 10.1111/nph.12247.PubMedPubMedCentralCrossRefGoogle Scholar
  28. Dimitri, P., Corradini, N., Rossi, F., & Vernì, F. (2005). The paradox of functional heterochromatin. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 27(1), 29–41. doi: 10.1002/bies.20158.CrossRefGoogle Scholar
  29. Dobson, F. S. (2013). The enduring question of sex-biased dispersal: Paul J. Greenwood’s (1980) seminal contribution. Animal Behaviour, 85(2), 299–304. doi: 10.1016/j.anbehav.2012.11.014.CrossRefGoogle Scholar
  30. Doolittle, W. F. (2013). Is junk DNA bunk? A critique of ENCODE. Proceedings of the National Academy of Sciences of the United States of America, 110(14), 5294–5300. doi: 10.1073/pnas.1221376110.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Doolittle, W. F., Brunet, T. D., Linquist, S., & Gregory, T. R. (2014). Distinguishing between “function” and “effect” in genome biology. Genome Biology and Evolution, 6(5), 1234–1237. doi: 10.1093/gbe/evu098.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Doolittle, W. F., & Sapienza, C. (1980). Selfish genes, the phenotype paradigm and genome evolution. Nature, 284(5757), 601–603. doi: 10.1038/284601a0.PubMedCrossRefGoogle Scholar
  33. Ehrenreich, I. M., & Pfennig, D. W. (2016). Genetic assimilation: A review of its potential proximate causes and evolutionary consequences. Ann Bot, 117(5), 769–779. doi: 10.1093/aob/mcv130.PubMedCrossRefGoogle Scholar
  34. Elgin, S. C., & Reuter, G. (2013). Position-effect variegation, heterochromatin formation, and gene silencing in Drosophila. Cold Spring Harbor Perspectives in Biology, 5(8), a017780. doi: 10.1101/cshperspect.a017780.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Ellegren, H. (2011). Sex-chromosome evolution: Recent progress and the influence of male and female heterogamety. Nature Reviews Genetics, 12(3), 157–166. doi: 10.1038/nrg2948.PubMedCrossRefGoogle Scholar
  36. Ellegren, H., & Parsch, J. (2007). The evolution of sex-biased genes and sex-biased gene expression. Nature Reviews Genetics, 8(9), 689–698. doi: 10.1038/nrg2167.PubMedCrossRefGoogle Scholar
  37. 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), 20140331. doi: 10.1098/rstb.2014.0331.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Feinberg, A. P., & Irizarry, R. A. (2010). Evolution in health and medicine Sackler colloquium: Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proceedings of the National Academy of Sciences of the United States of America, 107(Suppl 1), 1757–1764. doi: 10.1073/pnas.0906183107.PubMedCrossRefGoogle Scholar
  39. Folke, C. (2006). Resilience: The emergence of a perspective for social-ecological systems analyses. Global Environmental Change, 16(3), 253–267. doi: 10.1016/j.gloenvcha.2006.04.002.CrossRefGoogle Scholar
  40. Forsman, A. (2015). Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity, 115(4), 276–284. doi: 10.1038/hdy.2014.92.PubMedCrossRefGoogle Scholar
  41. Francisco, F. O., & Lemos, B. (2014). How do y-chromosomes modulate genome-wide epigenetic States: genome folding, chromatin sinks, and gene expression. Journal of Genomics, 2, 94–103. doi: 10.7150/jgen.8043.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Gallach, M., Domingues, S., & Betran, E. (2011). Gene duplication and the genome distribution of sex-biased genes. International Journal of Evolutionary Biology, 2011(3), 989438. doi: 10.4061/2011/989438.PubMedPubMedCentralGoogle Scholar
  43. Gamperl, R., Ehmann, C., & Bachmann, K. (1982). Genome size and heterochromatin variation in rodents. Genetica, 58(3), 199–212. doi: 10.1007/bf00128014.CrossRefGoogle Scholar
  44. Gemayel, R., Vinces, M. D., Legendre, M., & Verstrepen, K. J. (2010). Variable tandem repeats accelerate evolution of coding and regulatory sequences. Annual Review of Genetics, 44(1), 445–477. doi: 10.1146/annurev-genet-072610-155046.PubMedCrossRefGoogle Scholar
  45. Gibson, G., & Reed, L. K. (2008). Cryptic genetic variation. Current Biology, 18(21), R989–R990. doi: 10.1016/j.cub.2008.08.011.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Golic, K. G., Golic, M. M., & Pimpinelli, S. (1998). Imprinted control of gene activity in Drosophila. Current Biology, 8(23), 1273–1276. doi: 10.1016/S0960-9822(07)00537-4.PubMedCrossRefGoogle Scholar
  47. Graur, D., Zheng, Y., & Azevedo, R. B. (2015). An evolutionary classification of genomic function. Genome Biology and Evolution, 7(3), 642–645. doi: 10.1093/gbe/evv021.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Graur, D., Zheng, Y., Price, N., Azevedo, R. B., Zufall, R. A., & Elhaik, E. (2013). On the immortality of television sets: “Function” in the human genome according to the evolution-free gospel of ENCODE. Genome Biology and Evolution, 5(3), 578–590. doi: 10.1093/gbe/evt028.PubMedPubMedCentralCrossRefGoogle Scholar
  49. Greenwood, P. J. (1980). Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour, 28(4), 1140–1162. doi: 10.1016/s0003-3472(80)80103-5.CrossRefGoogle Scholar
  50. Gregory, T. R. (2002). Genome size and developmental complexity. Genetica, 115(1), 131–146. doi: 10.1023/A:1016032400147.PubMedCrossRefGoogle Scholar
  51. Gregory, T. R. (2003). Variation across amphibian species in the size of the nuclear genome supports a pluralistic, hierarchical approach to the C-value enigma. Biological Journal of the Linnean Society, 79(2), 329–339. doi: 10.1046/j.1095-8312.2003.00191.x.CrossRefGoogle Scholar
  52. Gregory, T. R. (2005). Synergy between sequence and size in large-scale genomics. Nature Reviews Genetics, 6(9), 699–708. doi: 10.1038/nrg1674.PubMedCrossRefGoogle Scholar
  53. Gregory, T. R. (2015). Animal genome size database. http://www.genomesize.com.http://www.genomesize.com.
  54. Gregory, T. R., & Johnston, J. S. (2008). Genome size diversity in the family Drosophilidae. Heredity, 101(3), 228–238. doi: 10.1038/hdy.2008.49.PubMedCrossRefGoogle Scholar
  55. Halfer, C. (1981). Interstrain heterochromatin polymorphisms in Drosophila melanogaster. Chromosoma, 84(2), 195–206. doi:  10.1007/BF00399131.PubMedCrossRefGoogle Scholar
  56. Hartmann-Goldstein, I. J. (2009). On the relationship between heterochromatization and variegation in Drosophila, with special reference to temperature sensitive periods. Genetical Research, 10(02), 143. doi: 10.1017/s0016672300010880.CrossRefGoogle Scholar
  57. Hughes, J. F., & Rozen, S. (2012). Genomics and genetics of human and primate y chromosomes. Annual Review of Genomics and Human Genetics, 13(1), 83–108. doi: 10.1146/annurev-genom-090711-163855.PubMedCrossRefGoogle Scholar
  58. IUCN Species Survival Commission. (2001). IUCN red list categories and criteria. Gland: IUCN.Google Scholar
  59. Jiang, Z. F., Croshaw, D. A., Wang, Y., Hey, J., & Machado, C. A. (2011). Enrichment of mRNA-like noncoding RNAs in the divergence of Drosophila males. Molecular Biology and Evolution, 28(4), 1339–1348. doi: 10.1093/molbev/msq293.PubMedCrossRefGoogle Scholar
  60. Joss, J. M. (2006). Lungfish evolution and development. General and Comparative Endocrinology, 148(3), 285–289. doi: 10.1016/j.ygcen.2005.10.010.PubMedCrossRefGoogle Scholar
  61. Jurka, J., Kapitonov, V. V., Kohany, O., & Jurka, M. V. (2007). Repetitive sequences in complex genomes: Structure and evolution. Annual Review of Genomics and Human Genetics, 8(1), 241–259. doi: 10.1146/annurev.genom.8.080706.092416.PubMedCrossRefGoogle Scholar
  62. Kaern, M., Elston, T. C., Blake, W. J., & Collins, J. J. (2005). Stochasticity in gene expression: From theories to phenotypes. Nature Reviews Genetics, 6(6), 451–464. doi: 10.1038/nrg1615.PubMedCrossRefGoogle Scholar
  63. Kapheim, K. M., Pan, H., Li, C., Salzberg, S. L., Puiu, D., Magoc, T., et al. (2015). Social evolution. Genomic signatures of evolutionary transitions from solitary to group living. Science, 348(6239), 1139–1143. doi: 10.1126/science.aaa4788.PubMedCrossRefGoogle Scholar
  64. Kashi, Y., & King, D. G. (2006). Simple sequence repeats as advantageous mutators in evolution. Trends in Genetics, 22(5), 253–259. doi: 10.1016/j.tig.2006.03.005.PubMedCrossRefGoogle Scholar
  65. Kellis, M., Wold, B., Snyder, M. P., Bernstein, B. E., Kundaje, A., Marinov, G. K., et al. (2014). Defining functional DNA elements in the human genome. Proceedings of the National Academy of Sciences of the United States of America, 111(17), 6131–6138. doi: 10.1073/pnas.1318948111.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kelly, S. A., Panhuis, T. M., & Stoehr, A. M. (2012). Phenotypic plasticity: molecular mechanisms and adaptive significance. Comprehensive Physiology, 2(2), 1417–1439. doi: 10.1002/cphy.c110008.PubMedGoogle Scholar
  67. Kerr, J. T., Pindar, A., Galpern, P., Packer, L., Potts, S. G., Roberts, S. M., et al. (2015). Climate change. Climate change impacts on bumblebees converge across continents. Science, 349(6244), 177–180. doi: 10.1126/science.aaa7031.PubMedCrossRefGoogle Scholar
  68. Kilfoil, M. L., Lasko, P., & Abouheif, E. (2009). Stochastic variation: from single cells to superorganisms. HFSP Journal, 3(6), 379–385. doi: 10.2976/1.3223356.PubMedPubMedCentralCrossRefGoogle Scholar
  69. King, D. G., Soller, M., & Kashi, Y. (1997). Evolutionary tuning knobs. Endeavour, 21(1), 36–40. doi: 10.1016/s0160-9327(97)01005-3.CrossRefGoogle Scholar
  70. Knight, C. A., Molinari, N. A., & Petrov, D. A. (2005). The large genome constraint hypothesis: Evolution, ecology and phenotype. Annals of Botany, 95(1), 177–190. doi: 10.1093/aob/mci011.PubMedPubMedCentralCrossRefGoogle Scholar
  71. Kraaijeveld, K. (2010). Genome size and species diversification. Evolutionary Biology, 37(4), 227–233. doi: 10.1007/s11692-010-9093-4.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Krsticevic, F. J., Schrago, C. G., & Carvalho, A. B. (2015). Long-read single molecule sequencing to resolve tandem gene copies: The Mst77Y region on the Drosophila melanogaster Y Chromosome. G3 (Bethesda), 5(6), 1145–1150. doi: 10.1534/g3.115.017277.CrossRefGoogle Scholar
  73. Lachaise, D., & Silvain, J.-F. (2004). How two Afrotropical endemics made two cosmopolitan human commensals: The Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica, 11(1–3), 17–39. doi: 10.1007/978-94-007-0965-2_2.CrossRefGoogle Scholar
  74. Lee, J., Alrubaian, J., & Dores, R. M. (2006). Are lungfish living fossils? Observation on the evolution of the opioid/orphanin gene family. General and Comparative Endocrinology, 148(3), 306–314. doi: 10.1016/j.ygcen.2006.07.010.PubMedCrossRefGoogle Scholar
  75. Lieber, M. R. (2010). The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annual Review of Biochemistry, 79(1), 181–211. doi: 10.1146/annurev.biochem.052308.093131.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Lyckegaard, E. M., & Clark, A. G. (1989). Ribosomal DNA and Stellate gene copy number variation on the Y chromosome of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 86(6), 1944–1948. doi: 10.1073/pnas.86.6.1944.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Lyckegaard, E. M., & Clark, A. G. (1991). Evolution of ribosomal RNA gene copy number on the sex chromosomes of Drosophila melanogaster. Molecular Biology and Evolution, 8(4), 458–474.PubMedGoogle Scholar
  78. Maggert, K. A., & Golic, K. G. (2002). The Y chromosome of Drosophila melanogaster exhibits chromosome-wide imprinting. Genetics, 162(3), 1245–1258. doi: 10.3410/f.1007729.179166.PubMedPubMedCentralGoogle Scholar
  79. Makarova, K. S., Aravind, L., Wolf, Y. I., Tatusov, R. L., Minton, K. W., Koonin, E. V., et al. (2001). Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiology and Molecular Biology Reviews, 65(1), 44–79. doi: 10.1128/MMBR.65.1.44-79.2001.PubMedPubMedCentralCrossRefGoogle Scholar
  80. Mank, J. E. (2009). Sex chromosomes and the evolution of sexual dimorphism: Lessons from the genome. The American Naturalist, 173(2), 141–150. doi: 10.1086/595754.PubMedCrossRefGoogle Scholar
  81. Mank, J. E. (2012). Small but mighty: The evolutionary dynamics of W and Y sex chromosomes. Chromosome Research, 20(1), 21–33. doi: 10.1007/s10577-011-9251-2.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Mank, J. E., & Avise, J. C. (2006). Cladogenetic correlates of genomic expansions in the recent evolution of actinopterygiian fishes. Proceedings of the Royal Society of London B: Biological Sciences, 273(1582), 33–38. doi: 10.1098/rspb.2005.3295.CrossRefGoogle Scholar
  83. Mank, J. E., Hultin-Rosenberg, L., Axelsson, E., & Ellegren, H. (2007). Rapid evolution of female-biased, but not male-biased, genes expressed in the avian brain. Molecular Biology and Evolution, 24(12), 2698–2706. doi: 10.1093/molbev/msm208.PubMedCrossRefGoogle Scholar
  84. Marcand, S., Gasser, S. M., & Gilson, E. (1996). Chromatin: A sticky silence. Current Biology, 6(10), 1222–1225. doi: 10.1016/S0960-9822(96)00701-4.PubMedCrossRefGoogle Scholar
  85. Markow, T. A., & O’Grady, P. (2005). Drosophila: A guide to species identification and use. London: Academic Press.Google Scholar
  86. Masel, J., & Trotter, M. V. (2010). Robustness and evolvability. Trends in Genetics, 26(9), 406–414. doi: 10.1016/j.tig.2010.06.002.PubMedPubMedCentralCrossRefGoogle Scholar
  87. McClintock, B. (1984). The significance of responses of the genome to challenge. Science, 226(4676), 792–801. doi: 10.1126/science.15739260.PubMedCrossRefGoogle Scholar
  88. Meisel, R. P. (2011). Towards a more nuanced understanding of the relationship between sex-biased gene expression and rates of protein-coding sequence evolution. Molecular Biology and Evolution, 28(6), 1893–1900. doi: 10.1093/molbev/msr010.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Moran, N. A., & Bennett, G. M. (2014). The tiniest tiny genomes. Annual Review of Microbiology, 68(1), 195–215. doi: 10.1146/annurev-micro-091213-112901.PubMedCrossRefGoogle Scholar
  90. Morris, J. J., Lenski, R. E., & Zinser, E. R. (2012). The Black Queen Hypothesis: Evolution of dependencies through adaptive gene loss. MBio, 3(2), e00036–e00012, doi: 10.1128/mBio.00036-12.PubMedPubMedCentralCrossRefGoogle Scholar
  91. National Research Council (2007). The limits of organic life in planetary systems. Washington, DC: The National Academies Press.Google Scholar
  92. Nei, M. (1972). Genetic distance between populations. The American Naturalist, 106(949), 283–292. doi: 10.1086/282771.
  93. Niu, D. K., & Jiang, L. (2013). Can ENCODE tell us how much junk DNA we carry in our genome? Biochemical and Biophysical Research Communications, 430(4), 1340–1343. doi: 10.1016/j.bbrc.2012.12.074.PubMedCrossRefGoogle Scholar
  94. Nonaka, E., Svanback, R., Thibert-Plante, X., Englund, G., & Brannstrom, A. (2015). Mechanisms by which phenotypic plasticity affects adaptive divergence and ecological speciation. The American Naturalist, 186(5), E126–E143. doi: 10.1086/683231.PubMedCrossRefGoogle Scholar
  95. Nova, P., Reutter, B. A., Rabova, M., & Zima, J. (2002). Sex-chromosome heterochromatin variation in the wood mouse, Apodemus sylvaticus. Cytogenetic and Genome Research, 96(1–4), 186–190. doi: 10.1159/000063033.PubMedCrossRefGoogle Scholar
  96. O’Meally, D., Patel, H. R., Stiglec, R., Sarre, S. D., Georges, A., Marshall Graves, J. A., et al. (2010). Non-homologous sex chromosomes of birds and snakes share repetitive sequences. Chromosome Research, 18(7), 787–800. doi: 10.1007/s10577-010-9152-9.PubMedCrossRefGoogle Scholar
  97. Ohno, S. (1972). So much “junk” DNA in our genome. Brookhaven Symposia in Biology, 23, 366–370.PubMedGoogle Scholar
  98. Oliver, K. R., & Greene, W. K. (2009). Transposable elements: Powerful facilitators of evolution. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 31(7), 703–714. doi: 10.1002/bies.200800219.CrossRefGoogle Scholar
  99. Oliver, M. J., Petrov, D., Ackerly, D., Falkowski, P., & Schofield, O. M. (2007). The mode and tempo of genome size evolution in eukaryotes. Genome Research, 17(5), 594–601. doi: 10.1101/gr.6096207.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Olmo, E. (2006). Genome size and evolutionary diversification in vertebrates. Italian Journal of Zoology, 73(2), 167–171. doi: 10.1080/11250000600680031.CrossRefGoogle Scholar
  101. Organ, C. L., Brusatte, S. L., & Stein, K. (2009). Sauropod dinosaurs evolved moderately sized genomes unrelated to body size. Proceedings of the Royal Society of London B: Biological Sciences, 276(1677), 4303–4308. doi: 10.1098/rspb.2009.1343.CrossRefGoogle Scholar
  102. Organ, C. L., Shedlock, A. M., Meade, A., Pagel, M., & Edwards, S. V. (2007). Origin of avian genome size and structure in non-avian dinosaurs. Nature, 446(7132), 180–184. doi: 10.1038/nature05621.PubMedCrossRefGoogle Scholar
  103. Orgel, L. E., & Crick, F. H. (1980). Selfish DNA: The ultimate parasite. Nature, 284(5757), 604–607. doi: 10.1038/284604a0.PubMedCrossRefGoogle Scholar
  104. Paaby, A. B., & Rockman, M. V. (2014). Cryptic genetic variation: Evolution’s hidden substrate. Nature Reviews Genetics, 15(4), 247–258. doi: 10.1038/nrg3688.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Palazzo, A. F., & Gregory, T. R. (2014). The case for junk DNA. PLoS Genetics, 10(5), e1004351. doi: 10.1371/journal.pgen.1004351.PubMedPubMedCentralCrossRefGoogle Scholar
  106. Papadopulos, A. S., Chester, M., Ridout, K., & Filatov, D. A. (2015). Rapid Y degeneration and dosage compensation in plant sex chromosomes. Proceedings of the National Academy of Sciences of the United States of America, 112(42), 13021–13026. doi: 10.1073/pnas.1508454112.PubMedPubMedCentralCrossRefGoogle Scholar
  107. Paredes, S., Branco, A. T., Hartl, D. L., Maggert, K. A., & Lemos, B. (2011). Ribosomal DNA deletions modulate genome-wide gene expression: “rDNA-sensitive” genes and natural variation. PLoS Genetics, 7(4), e1001376. doi: 10.1371/journal.pgen.1001376.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Parsch, J., & Ellegren, H. (2013). The evolutionary causes and consequences of sex-biased gene expression. Nature Reviews Genetics, 14(2), 83–87. doi: 10.1038/nrg3376.PubMedCrossRefGoogle Scholar
  109. Peng, J. C., & Karpen, G. H. (2007). H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nature Cell Biology, 9(1), 25–35. doi: 10.1038/ncb1514.PubMedCrossRefGoogle Scholar
  110. Perry, C. J., Sovik, E., Myerscough, M. R., & Barron, A. B. (2015). Rapid behavioral maturation accelerates failure of stressed honey bee colonies. Proceedings of the National Academy of Sciences of the United States of America, 112(11), 3427–3432. doi: 10.1073/pnas.1422089112.PubMedPubMedCentralCrossRefGoogle Scholar
  111. Peterson, B. K., Hare, E. E., Iyer, V. N., Storage, S., Conner, L., Papaj, D. R., et al. (2009). Big genomes facilitate the comparative identification of regulatory elements. PLoS One, 4(3), e4688. doi: 10.1371/journal.pone.0004688.PubMedPubMedCentralCrossRefGoogle Scholar
  112. Peterson, G., Allen, C. R., & Holling, C. S. (1998). Original articles: Ecological resilience, biodiversity, and scale. Ecosystems, 1(1), 6–18. doi: 10.1007/s100219900002.CrossRefGoogle Scholar
  113. Petit, R. J., & Excoffier, L. (2009). Gene flow and species delimitation. Trends in Ecology & Evolution (Personal Edition), 24(7), 386–393. doi: 10.1016/j.tree.2009.02.011.CrossRefGoogle Scholar
  114. Preston, C. R., Flores, C. C., & Engels, W. R. (2006). Differential usage of alternative pathways of double-strand break repair in Drosophila. Genetics, 172(2), 1055–1068. doi: 10.1534/genetics.105.050138.PubMedPubMedCentralCrossRefGoogle Scholar
  115. Raj, A., & van Oudenaarden, A. (2008). Nature, nurture, or chance: stochastic gene expression and its consequences. Cell, 135(2), 216–226. doi: 10.1016/j.cell.2008.09.050.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Raser, J. M., & O’Shea, E. K. (2005). Noise in gene expression: Origins, consequences, and control. Science, 309(5743), 2010–2013. doi: 10.1126/science.1105891.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Repping, S., van Daalen, S. K., Brown, L. G., Korver, C. M., Lange, J., Marszalek, J. D., et al. (2006). High mutation rates have driven extensive structural polymorphism among human Y chromosomes. Nature Genetics, 38(4), 463–467. doi: 10.1038/ng1754.PubMedCrossRefGoogle Scholar
  118. Richards, S., & Murali, S. C. (2015). Best practices in insect genome sequencing: What works and what doesn’t. Current Opinion in Insect Science, 7, 1–7. doi: 10.1016/j.cois.2015.02.013.PubMedPubMedCentralCrossRefGoogle Scholar
  119. Russo, C. A. M., Mello, B., Frazão, A., & Voloch, C. M. (2013). Phylogenetic analysis and a time tree for a large drosophilid data set (Diptera: Drosophilidae). Zoological Journal of the Linnean Society, 169(4), 765–775. doi: 10.1111/zoj.12062.CrossRefGoogle Scholar
  120. Sahara, K., Yoshido, A., & Traut, W. (2012). Sex chromosome evolution in moths and butterflies. Chromosome Research, 20(1), 83–94. doi: 10.1007/s10577-011-9262-z.PubMedCrossRefGoogle Scholar
  121. Schaafsma, S. M., & Pfaff, D. W. (2014). Etiologies underlying sex differences in Autism Spectrum Disorders. Frontiers in Neuroendocrinology, 35(3), 255–271. doi: 10.1016/j.yfrne.2014.03.006.PubMedCrossRefGoogle Scholar
  122. Schlichting, C. D., & Wund, M. A. (2014). Phenotypic plasticity and epigenetic marking: an assessment of evidence for genetic accommodation. Evolution, 68(3), 656–672. doi: 10.1111/evo.12348.PubMedCrossRefGoogle Scholar
  123. Sclavi, B., & Herrick, J. (2015). Ecological patterns of genome size variation and the origin of species in salamanders. https://arxiv.org/abs/1501.03782.
  124. Singh, L., Purdom, I. F., & Jones, K. W. (1980). Sex chromosome associated satellite DNA: evolution and conservation. Chromosoma, 79(2), 137–157.PubMedCrossRefGoogle Scholar
  125. Singh, R. S., & Artieri, C. G. (2010). Male sex drive and the maintenance of sex: evidence from Drosophila. Journal of Heredity, 101(Suppl 1), S100–S106. doi: 10.1093/jhered/esq006.PubMedCrossRefGoogle Scholar
  126. Smith, E. M., & Gregory, T. R. (2009). Patterns of genome size diversity in the ray-finned fishes. Hydrobiologia (Incorporating JAQU), 625(1), 1–25. doi: 10.1007/s10750-009-9724-x.CrossRefGoogle Scholar
  127. Staveley, J. P., Law, S. A., Fairbrother, A., & Menzie, C. A. (2014). A causal analysis of observed declines in managed honey bees (Apis mellifera). Human and Ecological Risk Assessment: An International Journal, 20(2), 566–591. doi: 10.1080/10807039.2013.831263.CrossRefGoogle Scholar
  128. Steinemann, S., & Steinemann, M. (2005). Retroelements: Tools for sex chromosome evolution. Cytogenetic and Genome Research, 110(1–4), 134–143. doi: 10.1159/000084945.PubMedCrossRefGoogle Scholar
  129. Suzuki, J., Yamaguchi, K., Kajikawa, M., Ichiyanagi, K., Adachi, N., Koyama, H., et al. (2009). Genetic evidence that the non-homologous end-joining repair pathway is involved in LINE retrotransposition. PLoS Genetics, 5(4), e1000461. doi: 10.1371/journal.pgen.1000461.PubMedPubMedCentralCrossRefGoogle Scholar
  130. Tadros, W., & Lipshitz, H. D. (2009). The maternal-to-zygotic transition: A play in two acts. Development (Cambridge, England), 136(18), 3033–3042. doi: 10.1242/dev.033183.CrossRefGoogle Scholar
  131. The Honeybee Genome Sequencing Consortium, Weinstock, G. M., Robinson, G. E., Gibbs, R. a., Worley, K. C., Evans, J. D., et al. (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature, 443(7), 931–949. doi: 10.1038/nature05260.PubMedCentralGoogle Scholar
  132. Throckmorton, L. H. (1975). The phylogeny, ecology, and geography of Drosophila (invertebrates of genetic interest). Boston: Springer.Google Scholar
  133. Tsutsui, N. D., Suarez, A. V., Spagna, J. C., & Johnston, J. S. (2008). The evolution of genome size in ants. BMC Evolutionary Biology, 8(1), 64. doi: 10.1186/1471-2148-8-64.PubMedPubMedCentralCrossRefGoogle Scholar
  134. van der Linde, K., Houle, D., Spicer, G. S., & Steppan, S. J. (2010). A supermatrix-based molecular phylogeny of the family Drosophilidae. Genetical Research, 92(1), 25–38. doi: 10.1017/S001667231000008X.CrossRefGoogle Scholar
  135. Vinogradov, A. E. (2003). Selfish DNA is maladaptive: Evidence from the plant Red List. Trends in Genetics, 19(11), 609–614. doi: 10.1016/j.tig.2003.09.010.PubMedCrossRefGoogle Scholar
  136. Vinogradov, A. E. (2004). Genome size and extinction risk in vertebrates. Proceedings of the Royal Society of London B: Biological Sciences, 271(1549), 1701–1705. doi: 10.1098/rspb.2004.2776.CrossRefGoogle Scholar
  137. Voss, S. R., Epperlein, H. H., & Tanaka, E. M. (2009). Ambystoma mexicanum, the axolotl: a versatile amphibian model for regeneration, development, and evolution studies. Cold Spring Harbor Protocols. doi: 10.1101/pdb.emo128.Google Scholar
  138. Voss, S. R., Woodcock, M. R., & Zambrano, L. (2015). A Tale of Two Axolotls. BioScience. doi: 10.1093/biosci/biv153.Google Scholar
  139. Watson, R. A., Mills, R., Buckley, C. L., Kouvaris, K., Jackson, A., Powers, S. T., et al. (2015). Evolutionary connectionism: Algorithmic principles underlying the evolution of biological organisation in evo-devo, evo-eco and evolutionary transitions. Evolutionary Biology. doi: 10.1007/s11692-015-9358-z.PubMedPubMedCentralGoogle Scholar
  140. Wijchers, P. J., Yandim, C., Panousopoulou, E., Ahmad, M., Harker, N., Saveliev, A., et al. (2010). Sexual dimorphism in mammalian autosomal gene regulation is determined not only by Sry but by sex chromosome complement as well. Developmental Cell, 19(3), 477–484. doi: 10.1016/j.devcel.2010.08.005.PubMedCrossRefGoogle Scholar
  141. Wolf, Y. I., & Koonin, E. V. (2013). Genome reduction as the dominant mode of evolution. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 35(9), 829–837. doi: 10.1002/bies.201300037.CrossRefGoogle Scholar
  142. Wyman, M. J., Agrawal, A. F., & Rowe, L. (2010). Condition-dependence of the sexually dimorphic transcriptome in Drosophila melanogaster. Evolution, 64(6), 1836–1848. doi: 10.1111/j.1558-5646.2009.00938.x.PubMedCrossRefGoogle Scholar
  143. Wyman, M. J., Cutter, A. D., & Rowe, L. (2012). Gene duplication in the evolution of sexual dimorphism. Evolution, 66(5), 1556–1566. doi: 10.1111/j.1558-5646.2011.01525.x.PubMedCrossRefGoogle Scholar
  144. Yassin, A. (2013). Phylogenetic classification of the Drosophilidae Rondani (Diptera): the role of morphology in the postgenomic era. Systematic Entomology, 38(2), 349–364. doi: 10.1111/j.1365-3113.2012.00665.x.CrossRefGoogle Scholar
  145. Yukilevich, R. (2012). Asymmetrical patterns of speciation uniquely support reinforcement in Drosophila. Evolution, 66(5), 1430–1446. doi: 10.1111/j.1558-5646.2011.01534.x.PubMedCrossRefGoogle Scholar
  146. Yun, A. J., Lee, P. Y., & Doux, J. D. (2006). Efficient inefficiency: Biochemical “junk” may represent molecular bridesmaids awaiting emergent function as a buffer against environmental fluctuation. Medical Hypotheses, 67(4), 914–921. doi: 10.1016/j.mehy.2006.02.022.PubMedCrossRefGoogle Scholar
  147. Zuckerkandl, E. (1974). A possible role of “inert” heterochromatin in cell differentiation. Action of and competition for “locking” molecules. Biochimie, 56(6–7), 937–954. doi: 10.1016/s0300-9084(74)80516-x.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.IrvineUSA

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