Skip to main content
SpringerLink
Log in

Hawaiian Drosophila genomes: size variation and evolutionary expansions

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

This paper reports genome sizes of one Hawaiian Scaptomyza and 16 endemic Hawaiian Drosophila species that include five members of the antopocerus species group, one member of the modified mouthpart group, and ten members of the picture wing clade. Genome size expansions have occurred independently multiple times among Hawaiian Drosophila lineages, and have resulted in an over 2.3-fold range of genome sizes among species, with the largest observed in Drosophila cyrtoloma (1C = 0.41 pg). We find evidence that these repeated genome size expansions were likely driven by the addition of significant amounts of heterochromatin and satellite DNA. For example, our data reveal that the addition of seven heterochromatic chromosome arms to the ancestral haploid karyotype, and a remarkable proportion of ~70 % satellite DNA, account for the greatly expanded size of the D. cyrtoloma genome. Moreover, the genomes of 13/17 Hawaiian picture wing species are composed of substantial proportions (22–70 %) of detectable satellites (all but one of which are AT-rich). Our results suggest that in this tightly knit group of recently evolved species, genomes have expanded, in large part, via evolutionary amplifications of satellite DNA sequences in centric and pericentric domains (especially of the X and dot chromosomes), which have resulted in longer acrocentric chromosomes or metacentrics with an added heterochromatic chromosome arm. We discuss possible evolutionary mechanisms that may have shaped these patterns, including rapid fixation of novel expanded genomes during founder-effect speciation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abad JP, Carmena M, Baars S, Saunders RD, Glover DM, Ludena P, Sentis C, Tyler-Smith C, Villasante A (1992) Dodeca satellite: a conserved G + C rich satellite from the centromeric heterochromatin of Drosophila melanogaster. Proc Natl Acad Sci USA 89:4663–4667

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Adams MD, Celniker SE, Holt RA et al (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195

    Article  PubMed  Google Scholar 

  • Appels R, Peacock WJ (1978) The arrangement and evolution of highly repeated (satellite) DNA sequences with special reference to Drosophila. Int Rev Cytol Suppl 8:69–126

    Article  PubMed  CAS  Google Scholar 

  • Baker R, DeSalle R (1997) Multiple sources of character evolution and the phylogeny of Hawaiian drosophilids. Syst Biol 46(4):654–673

    Article  PubMed  CAS  Google Scholar 

  • Bensasson D, Petrov DA, Zhang DX, Hartl DL, Hewitt GM (2001) Genomic gigantism: DNA loss is slow in mountain grasshoppers. Mol Biol Evol 18:246–253

    Article  PubMed  CAS  Google Scholar 

  • Bergman CM, Quesneville H, Anxolabéhère D, Ashburner M (2006) Recurrent insertion and duplication generate networks of transposable element sequences in the Drosophila melanogaster genome. Genome Biol 7:R112

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Biémont C, Vieira C (2005) What transposable elements tell us about genome organization and evolution: the case of Drosophila. Cytogenet Genome Res 110:25–34

    Article  PubMed  CAS  Google Scholar 

  • Biémont C, Vieira C (2006) Junk DNA as an evolutionary force. Nature 443:521–524

    Article  PubMed  CAS  Google Scholar 

  • Biessmann H, Zurovcova M, Yao JG, Lozovskaya E, Walter MF (2000) A telomeric satellite in Drosophila virilis and its sibling species. Chromosoma 109:372–380

    Article  PubMed  CAS  Google Scholar 

  • Bonaccorsi S, Lohe A (1991) Fine mapping of satellite DNA sequences along the Y chromosome of Drosophila melanogaster: relationships between satellite sequences and fertility factors. Genetics 129:177–189

    PubMed Central  PubMed  CAS  Google Scholar 

  • Bonacum J, O’Grady PM, Kambysellis MP, DeSalle R (2005) Phylogeny and age of diversification of the planitibia species group of the Hawaiian Drosophila. Molec Phylog Evol 37:73–82

    Article  CAS  Google Scholar 

  • Bosco G, Campbell P, Leiva-Neto JT, Markow TA (2007) Analysis of Drosophila species genome size and satellite DNA content reveals significant differences among strains as well as between species. Genetics 177:1277–1290

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Boulesteix M, Weiss M, Biémont C (2006) Differences in genome size between closely related species: the Drosophila melanogaster species subgroup. Mol Biol Evol 23:162–167

    Article  PubMed  CAS  Google Scholar 

  • Burrack LS, Berman J (2012) Flexibility of centromere and kinetochore structures. Trends Genet 28:204–212

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Carson HL (1971) Speciation and the founder principle. Stadler Genet Symp 3:51–70

    Google Scholar 

  • Carson HL (1983) Chromosomal sequences and interisland colonization in Hawaiian Drosophila. Genetics 103:465–482

    PubMed Central  PubMed  CAS  Google Scholar 

  • Carson HL, Clague DA (1995) Geology and biogeography of the Hawaiian islands. In: Wagner WL, Funk VA (eds) Hawaiian biogeography. Smithsonian Institution Press, Washington, pp 14–29

    Google Scholar 

  • Carson HL, Templeton AR (1984) Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annu Rev Ecol Syst 15:97–131

    Article  Google Scholar 

  • Carson HL, Lockwood JP, Craddock EM (1990) Extinction and recolonization of local populations on a growing shield volcano. Proc Natl Acad Sci USA 87:7055–7057

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Celniker SE, Rubin GM (2003) The Drosophila melanogaster genome. Annu Rev Genomics Hum Genet 4:89–117

    Article  PubMed  CAS  Google Scholar 

  • Chang LS, Carson HL (1985) Metaphase karyotype identity in four homosequential Drosophila species from Hawaii. Can J Genet Cytol 27:308–311

    Article  Google Scholar 

  • Charlesworth B, Barton N (2004) Genome size: does bigger mean worse? Curr Biol 14:R233–R235

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth B, Jarne P, Assimacopoulos S (1994a) The distribution of transposable elements within and between chromosomes in a population of Drosophila melanogaster. III. Element abundances in heterochromatin. Genet Res 64:183–197

    Article  PubMed  CAS  Google Scholar 

  • Charlesworth B, Sniegowsky P, Stephan W (1994b) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220

    Article  PubMed  CAS  Google Scholar 

  • Clayton FE (1966) Preliminary report on the karyotypes of Hawaiian Drosophilidae. Univ Texas Publ 6615:397–404

    Google Scholar 

  • Clayton FE (1969) Variations in the metaphase chromosomes of Hawaiian Drosophilidae. Univ Texas Publ 6918:95–110

    Google Scholar 

  • Clayton FE (1985) The meiotic and mitotic chromosomes of picture-winged Hawaiian Drosophila species. I. Drosophila grimshawi and D. cyrtoloma. Can J Genet Cytol 27(4):441–449

    Article  PubMed  CAS  Google Scholar 

  • Clayton FE (1988) The role of heterochromatin in karyotype variation among Hawaiian picture-winged Drosophila. Pac Sci 42:28–47

    Google Scholar 

  • Clayton FE, Guest WC (1986) Overview of chromosomal evolution in the family Drosophilidae. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology of Drosophila, vol 3e. Academic Press, London, pp 1–38

    Google Scholar 

  • Clayton FE, Wheeler MR (1975) A catalog of Drosophila metaphase chromosome configurations. In: King RC (ed) Handbook of genetics, vol 3. Plenum Press, New York, pp 471–512

    Google Scholar 

  • Cordeiro M, Wheeler L, Lee CS, Kastritsis CD, Richardson RH (1975) Heterochromatic chromosomes and satellite DNAs of Drosophila nasutoides. Chromosoma 51:65–73

    Article  PubMed  CAS  Google Scholar 

  • Cordeiro-Stone M, Lee CS (1976) Studies on the satellite DNAs of Drosophila nasutoides: their buoyant densities, melting temperatures, reassociation rates and localizations in polytene chromosomes. J Mol Biol 104:1–24

    Article  PubMed  CAS  Google Scholar 

  • Cuadrado A, Jouve N (2011) Novel simple sequence repeats (SSRs) detected by ND-FISH in heterochromatin of Drosophila melanogaster. BMC Genomics 12:205

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603

    Article  PubMed  CAS  Google Scholar 

  • Drosophila 12 Genomes Consortium (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203–218

    Article  CAS  Google Scholar 

  • Endow SA, Polan ML, Gall JG (1975) Satellite DNA sequences of Drosophila melanogaster. J Mol Biol 96(4):665–674

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125(1):1–15

    Article  Google Scholar 

  • Ferree PM, Barbash DA (2009) Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol 7(10):e1000234. doi:10.1371/journal.pbio.1000234

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ferree PM, Prasad S (2012) How can satellite DNA divergence cause reproductive isolation? Let us count the chromosomal ways. Genet Res Int. doi:10.1155/2012/430136

    PubMed Central  PubMed  Google Scholar 

  • Gall JG, Atherton DD (1974) Satellite DNA sequences in Drosophila virilis. J Mol Biol 85:633–664

    Article  PubMed  CAS  Google Scholar 

  • Gall JG, Cohen EH, Polan ML (1971) Repetitive DNA sequences in Drosophila. Chromosoma 33:319–344

    Article  PubMed  CAS  Google Scholar 

  • Gallach M (2014) Recurrent turnover of chromosome-specific satellites in Drosophila. Genome Biol Evol 6(6):1279–1286

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • González J, Petrov DA (2009) The adaptive role of transposable elements in the Drosophila genome. Gene 448:124–133

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gregory TR (2015) Animal genome size database (release 2.0). http://www.genomesize.com

  • Gregory TR, Johnston JS (2008) Genome size diversity in the family Drosophilidae. Heredity 101:228–238

    Article  PubMed  CAS  Google Scholar 

  • Hawkins JS, Grover CE, Wendel JF (2008) Repeated big bangs and the expanding universe: directionality in plant genome size evolution. Plant Sci 174:557–562

    Article  CAS  Google Scholar 

  • He B, Caudy A, Parsons L, Rosebrock A, Pane A, Raj S, Wieschaus E (2012) Mapping the pericentric heterochromatin by comparative genomic hybridization analysis and chromosome deletions in Drosophila melanogaster. Genome Res 22:2507–2519

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Heikkinen E, Launonen V, Muller E, Bachmann L (1995) The pvB370 BamHI satellite DNA family of the Drosophila virilis group and its evolutionary relation to mobile dispersed genetic pDv elements. J Mol Evol 41:604–614

    Article  PubMed  CAS  Google Scholar 

  • Hennig W (1999) Heterochromatin. Chromosoma 108:1–9

    Article  PubMed  CAS  Google Scholar 

  • Hennig W, Hennig I, Stein H (1970) Repeated sequences in the DNA of Drosophila and their localization in giant chromosomes. Chromosoma 32(1):31–63

    Article  PubMed  CAS  Google Scholar 

  • Hoskins RA, Smith CD, Carlson JW, Carvalho AB, Halpern A et al (2002) Heterochromatic sequences in a Drosophila whole genome shotgun assembly. Genome Biol 3(12):0085.1–0085.16

    Article  Google Scholar 

  • Hoskins RA, Carlson JW, Kennedy C, Acevedo D, Evans-Holm M, Frise E et al (2007) Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 15:1625–1628

    Article  CAS  Google Scholar 

  • Hoskins RA, Carlson JW, Wan KH, Park S, Mendez I, Galle SE et al (2015) The Release 6 reference sequence of the Drosophila melanogaster genome. Genome Res 25:445–458

    Article  PubMed Central  PubMed  Google Scholar 

  • Hsieh T, Brutlag D (1979) Sequence and sequence variation within the 1.688 g/cm3 satellite DNA of Drosophila melanogaster. J Mol Biol 135(2):465–481

    Article  PubMed  CAS  Google Scholar 

  • Kacmarczyk Th, Craddock EM (2000) Cell size is a factor in body size variation among Hawaiian and non Hawaiian species of Drosophila. Dros Inf Serv 83:144–148 (plus Corrigendum: Dros Inf Serv 85:171)

    Google Scholar 

  • Kambysellis MP, Craddock EM (1997) Ecological and reproductive shifts in the diversification of the endemic Hawaiian Drosophila. In: Givnish TJ, Sytsma KJ (eds) Molecular evolution and adaptive radiation. Cambridge Univ Press, Cambridge, pp 475–509

    Google Scholar 

  • Kambysellis MP, Ho K-F, Craddock EM, Piano F, Parisi M, Cohen J (1995) Pattern of ecological shifts in the diversification of Hawaiian Drosophila inferred from a molecular phylogeny. Curr Biol 5(10):1129–1139

    Article  PubMed  CAS  Google Scholar 

  • Kaneshiro KY (1997) R.C.L. Perkins’ legacy to evolutionary research on Hawaiian Drosophilidae (Diptera). Pac Sci 51:450–461

    Google Scholar 

  • Kapitonov VV, Jurka J (2003) Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proc Natl Acad Sci USA 100:6569–6574

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kidwell MG (2002) Transposable elements and the evolution of genome size in eukaryotes. Genetica 115:49–63

    Article  PubMed  CAS  Google Scholar 

  • Kidwell MG, Lisch DR (2000) Transposable elements and host genome evolution. Trends Ecol Evol 15:95–99

    Article  PubMed  Google Scholar 

  • Kidwell MG, Lisch DR (2001) Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55:1–24

    Article  PubMed  CAS  Google Scholar 

  • Kloc A, Martienssen R (2008) RNAi, heterochromatin and the cell cycle. Trends Genet 24(10):511–517. doi:10.1016/j.tig.2008.08.002

    Article  PubMed  CAS  Google Scholar 

  • Kuhn GCS (2015) Satellite DNA transcripts have diverse biological roles in Drosophila. Heredity 115:1–2. doi:10.1038/hdy.2015.12

    Article  PubMed  CAS  Google Scholar 

  • Lamb JC, Theuri J, Birchler JA (2004) What’s in a centromere? Genome Biol 5:239

    Article  PubMed Central  PubMed  Google Scholar 

  • Lapoint RT, Magnacca KN, O’Grady PM (2014) Phylogenetics of the antopocerus-modified tarsus clade of Hawaiian Drosophila: diversification across the Hawaiian islands. PLoS One 9(11):e113227

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lemeunier F, Dutrillaux B, Ashburner M (1978) Relationships within the melanogaster subgroup species of the genus Drosophila (Sophophora). III. The mitotic chromosomes and quinacrine fluorescent patterns of the polytene chromosomes. Chromosoma 69:349–361

    Article  Google Scholar 

  • Levasseur A, Pontarotti P (2011) The role of duplications in the evolution of genomes highlights the need for evolutionary-based approaches in comparative genomics. Biol Direct 6:11

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4(3):203–221

    PubMed  CAS  Google Scholar 

  • Lohe AR, Brutlag DL (1986) Multiplicity of satellite DNA sequences in Drosophila melanogaster. Proc Natl Acad Sci USA 83:696–700

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lohe AR, Brutlag DL (1987) Identical satellite DNA sequences in sibling species of Drosophila. J Mol Biol 194(2):161–170

    Article  PubMed  CAS  Google Scholar 

  • Lynch M (2007a) The origins of genome architecture. Sinauer Assoc. Inc, Sunderland

    Google Scholar 

  • Lynch M (2007b) The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci USA 104(Suppl 1):8597–8604

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lynch M, Connery JS (2003) The origins of genome complexity. Science 302:1401–1404

    Article  PubMed  CAS  Google Scholar 

  • Ma J, Jackson SA (2006) Retrotransposon accumulation and satellite amplification mediated by segmental duplication facilitate centromere expansion in rice. Genome Res 16:251–259

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Magnacca KN, Price DK (2015) Rapid adaptive radiation and host plant conservation in the Hawaiian picture wing Drosophila (Diptera: Drosophilidae). Mol Phylogenet Evol 92:226–242

    Article  PubMed  Google Scholar 

  • Malik HS, Henikoff S (2002) Conflict begets complexity: the evolution of centromeres. Curr Opin Genet Dev 12:711–718

    Article  PubMed  CAS  Google Scholar 

  • Mandel M, Schildkraut CL, Marmur J (1968) Use of CsCl density gradient analysis for determining the guanine plus cytosine content of DNA. In: Grossman L, Moldave K (eds) Methods in enzymology XIIB. Academic Press, New York, pp 184–195

    Google Scholar 

  • Maumus F, Fiston-Lavier A, Quesneville H (2015) Impact of transposable elements on insect genomes and biology. Curr Opin Insect Sci 7:30–36

    Article  Google Scholar 

  • Miklos GLG, Gill AC (1981) The DNA sequences of cloned complex satellite DNAs from Hawaiian Drosophila and their bearing on satellite DNA sequence conservation. Chromosoma 82:409–427

    Article  PubMed  CAS  Google Scholar 

  • Morales-Hojas R, Vieira J (2012) Phylogenetic patterns of geographical and ecological diversification in the subgenus Drosophila. PLoS One 7(11):e49552

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • O’Grady PM, DeSalle R (2008) Out of Hawaii: the origin and biogeographic history of the genus Scaptomyza (Diptera, Drosophilidae). Biol Lett 4(2):195–199

    Article  PubMed Central  PubMed  Google Scholar 

  • O’Grady PM, Bonacum J, DeSalle R, Do Val F (2003) The placement of Engiscaptomyza Grimshawomyia, and Titanochaeta, three clades of endemic Hawaiian Drosophilidae (Diptera). Zootaxa 159:1–16

    Google Scholar 

  • O’Grady PM, Magnacca KN, Lapoint RT (2010) Taxonomic relationships within the endemic Hawaiian Drosophilidae. Rec Hawaii Biol Surv 108:3–35

    Google Scholar 

  • O’Grady PM, Lapoint RT, Bonacum J, Lasola J, Owen E, Wu Y, DeSalle R (2011) Phylogenetic and ecological relationships of the Hawaiian Drosophila inferred by mitochondrial DNA analysis. Mol Phylogenet Evol 58(2):244–256

    Article  PubMed  CAS  Google Scholar 

  • Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607

    Article  PubMed  CAS  Google Scholar 

  • Pal-Bhadra M, Leibovitch BA, Gandhi SG, Rao M, Bhadra U, Birchler JA, Elgin SC (2004) Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303:669–672

    Article  PubMed  CAS  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20(2):289–290

    Article  PubMed  CAS  Google Scholar 

  • Petrov DA (2001) Evolution of genome size: new approaches to an old problem. Trends Genet 17:23–28

    Article  PubMed  CAS  Google Scholar 

  • Petrov DA (2002) DNA loss and evolution of genome size in Drosophila. Genetica 115:81–91

    Article  PubMed  CAS  Google Scholar 

  • Petrov DA, Sangster TA, Johnston JS, Hartl DL, Shaw KL (2000) Evidence for DNA loss as a determinant of genome size. Science 287:1060–1062

    Article  PubMed  CAS  Google Scholar 

  • Pezer Z, Brajković J, Feliciello I, Ugarković D (2011) Transcription of satellite DNAs in insects. Prog Mol Subcell Biol 51:161–178

    Article  PubMed  CAS  Google Scholar 

  • Pidoux AL, Allshire RC (2005) The role of heterochromatin in centromere function. Philos Trans R Soc Lond B Biol Sci 360:569–579

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Piegu B, Guyot R, Picault N, Roulin A, Sanyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA, Panaud O (2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16:1262–1269

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pimpinelli S, Berloco M, Fanti L, Dimitri P, Bonaccorsi S, Marchetti E, Caizzi R, Caggese C, Gatti M (1995) Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc Natl Acad Sci USA 92:3804–3808

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rasch EM (1985) DNA ‘‘standards’’ and the range of accurate DNA estimates by Feulgen absorption microspectrophotometry. In: Cowden RR, Harrison SH (eds) Advances in microscopy. Alan R Liss, New York, pp 137–166

    Google Scholar 

  • Remsen J, O’Grady P (2002) Phylogeny of Drosophilinae (Diptera:Drosophilidae), with comments on combined analysis and character support. Mol Phylogenet Evol 24:249–264

    Article  PubMed  Google Scholar 

  • Rošić S, Köhler F, Erhardt S (2014) Repetitive centromeric satellite RNA is essential for kinetochore formation and cell division. J Cell Biol 207(3):335–349

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Russo CAM, Takezaki N, Nei M (1995) Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol 12:391–404

    PubMed  CAS  Google Scholar 

  • Russo CAM, Mello B, Frazao A, Voloch CM (2013) Phylogenetic analysis and a time tree for a large drosophilid data set (Diptera: Drosophilidae). Zool J Linn Soc 169:765–775

    Article  Google Scholar 

  • Schaeffer SW, Bhutkar A, McAllister BF, Matsuda M, Matzkin LM et al (2008) Polytene chromosome maps of 11 Drosophila species: the order of genomic scaffolds inferred from genetic and physical maps. Genetics 179:1601–1655

    Article  PubMed Central  PubMed  Google Scholar 

  • Schueler MG, Dunn JM, Bird CP, Ross MT, Viggiano L et al (2005) Progressive proximal expansion of the primate X chromosome centromere. Proc Nat Acad Sci USA 102:10563–10568

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schweber MS (1974) The satellite bands of the DNA of Drosophila virilis. Chromosoma 44:371–382

    Article  PubMed  CAS  Google Scholar 

  • Shapiro JA, von Sternberg R (2005) Why repetitive DNA is essential to genome function. Biol Rev 80:227–250

    Article  PubMed  Google Scholar 

  • Singh ND, Petrov DA (2004) Rapid sequence turnover at an intergenic locus in Drosophila. Mol Biol Evol 21(4):670–680

    Article  PubMed  CAS  Google Scholar 

  • Slawson EE, Shaffer CD, Malone CD, Leung W, Kellmann E, Shevchek RB et al (2006) Comparison of dot chromosome sequences from D. melanogaster and D. virilis reveals an enrichment of DNA transposon sequences in heterochromatic domains. Genome Biol 7:R15. doi:10.1186/gb-2006-7-2-r15

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Smith GP (1976) Evolution of repeated DNA sequences by unequal crossing-over. Science 191:528–535

    Article  PubMed  CAS  Google Scholar 

  • Strachan T, Coen E, Webb D, Dover G (1982) Modes and rates of change of complex DNA families of Drosophila. J Mol Biol 158:37–54

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Le HD, Wahlstrom JM, Karpen GH (2003) Sequence analysis of a functional Drosophila centromere. Genome Res 13:182–194

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Templeton AR (1980) The theory of speciation via the founder principle. Genetics 94:1011–1038

    PubMed Central  PubMed  CAS  Google Scholar 

  • Templeton AR (2008) The reality and importance of founder speciation in evolution. BioEssays 30:470–479

    Article  PubMed  Google Scholar 

  • Ugarković D, Plohl M (2002) Variation in satellite DNA profiles—causes and effects. EMBO J 21:5955–5959

    Article  PubMed  Google Scholar 

  • Usakin L, Abad J, Vagin VV, De Pablos B, Villasante A, Gvozdev VA (2007) Transcription of the 1.688 satellite DNA family is under the control of RNA interference machinery in Drosophila melanogaster ovaries. Genetics 176:1343–1349

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vinogradov AE (2004) Evolution of genome size: multilevel selection, mutation bias or dynamical chaos? Curr Opin Genet Dev 14:620–626

    Article  PubMed  CAS  Google Scholar 

  • Westerman M, Barton NH, Hewitt GM (1987) Differences in DNA content between two chromosomal races of the grasshopper Podisma pedestris. Heredity 58:221–228

    Article  Google Scholar 

  • Whitney KD, Garland T Jr (2010) Did genetic drift drive increases in genome complexity? PLoS Genet 6(8):e1001080

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Whitney KD, Boussau B, Baack EJ, Garland T Jr (2011) Drift and genome complexity revisited. PLoS Genet 7(6):e1002092

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yoon JS, Richardson RH (1976) Evolution of Hawaiian Drosophilidae: II. Patterns and rates of chromosome evolution in an antopocerus phylogeny. Genetics 83:827–843

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yoon JS, Richardson RH (1978) Evolution in Hawaiian Drosophilidae III. The microchromosome and heterochromatin of Drosophila. Evolution 32:475–484

    Article  Google Scholar 

  • Zacharias H (1986) Tissue-specific schedule of selective replication in Drosophila nasutoides. Roux’s Arch Dev Biol 195:378–388

    Article  Google Scholar 

Download references

Acknowledgments

To Robert Dawley of Ursinus College, Collegeville, PA, sincere thanks for use of his flow cytometer, and for sharing his data on Drosophila silvarentis. My late husband Michael Kambysellis helped enormously with processing the samples for flow cytometry, as well as with the field collections. Much appreciation goes to Purchase colleague Susan Letcher for generously sharing her expertise to facilitate the phylogenetic analyses. Thanks also to Ken Kaneshiro of the University of Hawaii for confirming identities of the field material, and to the reviewers for their comments. For permits to collect specimens of Hawaiian Drosophila from the field, I am grateful to the following: State of Hawaii Department of Land and Natural Resources/Hawaii Natural Area Reserves System, The Nature Conservancy of Hawaii, U.S. Department of the Interior, National Park Service, and the U.S. Fish and Wildlife Service, National Wildlife Refuge. I also acknowledge the East Maui Irrigation Co. Ltd. for a Right of Entry Agreement that enabled collections in Waikamoi Forest Preserve.

Funding

Most of this study was funded by National Science Foundation Grant DEB97-29192 to EMC. The satDNA analyses were supported by ACS Grant VC-85 to JGG.

Author information

Authors and Affiliations

  1. Natural Sciences Building, Purchase College, State University of New York, 735 Anderson Hill Road, Purchase, NY, 10577, USA

    Elysse M. Craddock & Mark Jonas

  2. Department of Embryology, Carnegie Institution for Science, Baltimore, MD, USA

    Joseph G. Gall

Authors
  1. Elysse M. Craddock
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph G. Gall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark Jonas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elysse M. Craddock.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 3025 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Craddock, E.M., Gall, J.G. & Jonas, M. Hawaiian Drosophila genomes: size variation and evolutionary expansions. Genetica 144, 107–124 (2016). https://doi.org/10.1007/s10709-016-9882-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-016-9882-5

Keywords

Search

Navigation