Abstract
Chromosome rearrangements have been implicated in diseases, such as cancer, and speciation, but it remains unclear whether rearrangements are causal or merely a consequence of these processes. Two marsupial families with very different rates of karyotype evolution provide excellent models in which to study the role of chromosome rearrangements in a disease and evolutionary context. The speciose family Dasyuridae displays remarkable karyotypic conservation, with all species examined to date possessing nearly identical karyotypes. Despite the seemingly high degree of chromosome stability within this family, they appear prone to developing tumours, including transmissible devil facial tumours. In contrast, chromosome rearrangements have been frequent in the evolution of the species-rich family Macropodidae, which displays a high level of karyotypic diversity. In particular, the genus Petrogale (rock-wallabies) displays an extraordinary level of chromosome rearrangement among species. For six parapatric Petrogale species, it appears that speciation has essentially been caught in the act, providing an opportunity to determine whether chromosomal rearrangements are a cause or consequence of speciation in this system. This review highlights the reasons that these two marsupial families are excellent models for testing hypotheses for hotspots of chromosome rearrangement and deciphering the role of chromosome rearrangements in disease and speciation.
Similar content being viewed by others
References
Agar WE (1923) The male meiotic phase in two genera of marsupials (Macropus and Petauroides). Quaterly J Microsc Sci s2-67:183–202
Alsop AE, Miethke P, Rofe R et al (2005) Characterizing the chromosomes of the Australian model marsupial Macropus eugenii (tammar wallaby). Chromosom Res 13:627–636. doi:10.1007/s10577-005-0989-2
Bailey JA, Eichler EE (2006) Primate segmental duplications: crucibles of evolution, diversity and disease. Nat Rev Genet 7:552–64. doi:10.1038/nrg1895
Barrick JE, Lenski RE (2013) Genome dynamics during experimental evolution. Nat Rev Genet 14:827–39. doi:10.1038/nrg3564
Bender HS, Murchison EP, Pickett HA et al (2012) Extreme telomere length dimorphism in the Tasmanian devil and related marsupials suggests parental control of telomere length. PLoS One. doi:10.1371/journal.pone.0046195
Brown JD, O’Neill RJ (2010) Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. Annu Rev Genomics Hum Genet 11:291–316. doi:10.1146/annurev-genom-082509-141554
Bulazel KV, Ferreri GC, Eldridge MDB, O’Neill RJ (2007) Species-specific shifts in centromere sequence composition are coincident with breakpoint reuse in karyotypically divergent lineages. Genome Biol 8:R170. doi:10.1186/gb-2007-8-8-r170
Canfield PJ, Cunningham AA (1993) Disease and mortality in Australasian marsupials held at London Zoo, 1872-1972. J Zoo Wildl Med 24:158–167
Canfield PJ, Hartley WJ, Reddacliff GL (1990) Spontaneous proliferations in Australian marsupials—a survey and review. 2. Dasyurids and bandicoots. J Comp Pathol 103:147–158
Capozzi O, Carbone L, Stanyon RR et al (2012) A comprehensive molecular cytogenetic analysis of chromosome rearrangements in gibbons. Genome Res 22:2520–2528. doi:10.1101/gr.138651.112
Carbone L, Harris RA, Vessere GM et al (2009) Evolutionary breakpoints in the gibbon suggest association between cytosine methylation and karyotype evolution. PLoS Genet. doi:10.1371/journal.pgen.1000538
Cesare AJ, Reddel RR (2008) Telomere uncapping and alternative lengthening of telomeres. Mech Ageing Dev 129:99–108. doi:10.1016/j.mad.2007.11.006
Close RL, Bell JN (1997) Fertile hybrids in two genera of wallabies: Petrogale and Thylogale. J Hered 88:393–397
Close RL, Lowry PS (1990) Hybrids in marsupial research. Aust J Zool 37:259–267
Darai E, Kost-Alimova M, Kiss H et al (2005) Evolutionarily plastic regions at human 3p21.3 coincide with tumor breakpoints identified by the “elimination test.”. Genomics 86:1–12. doi:10.1016/j.ygeno.2005.04.003
Darai-Ramqvist E, Sandlund A, Müller S et al (2008) Segmental duplications and evolutionary plasticity at tumor chromosome break-prone regions. Genome Res 18:370–379. doi:10.1101/gr.7010208
Das U, Das AK (2000) Review of canine transmissible venereal sarcoma. Vet Res Commun 24:545–556. doi:10.1023/A:1006491918910
Deakin JE, Bender HS, Pearse AM, et al. (2012a) Genomic restructuring in the Tasmanian devil facial tumour: chromosome painting and gene mapping provide clues to evolution of a transmissible tumour. PLoS Genet 8:e1002483. doi: 10.1371/journal.pgen.1002483
Deakin JE, Delbridge ML, Koina E et al (2013) Reconstruction of the ancestral marsupial karyotype from comparative gene maps. BMC Evol Biol 13:258. doi:10.1186/1471-2148-13-258
Deakin JE, Graves JAM, Rens W (2012b) The evolution of marsupial and monotreme chromosomes. Cytogenet Genome Res 137:113–29. doi: 10.1159/000339433
Deakin JE, Koina E, Waters PD et al (2008) Physical map of two tammar wallaby chromosomes: a strategy for mapping in non-model mammals. Chromosom Res 16:1159–1175. doi:10.1007/s10577-008-1266-y
Duke Becker SE, Thomas R, Trifonov VA et al (2011) Anchoring the dog to its relatives reveals new evolutionary breakpoints across 11 species of the Canidae and provides new clues for the role of B chromosomes. Chromosom Res 19:685–708. doi:10.1007/s10577-011-9233-4
Eldridge MDB, Close RL (1993) Radiation of chromosome shuffles. Curr Opin Genet Dev 3:915–922. doi:10.1016/0959-437X(93)90014-G
Eldridge MDB, Close RL, Johnston PG (1990) Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia, Macropodidae).III. G-banding analysis of Petrogale lateralis inornata and P. penicillata. Genome 33:798–802
Eldridge MDB, Close RL, Johnston PG (1991) Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia, Macropodidae).IV. G-banding analysis of the Petrogale lateralis complex. Aust J Zool 39:621–627. doi:10.1071/ZO991062
Eldridge MDB, Dollin AE, Johnston PG et al (1988) Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia; Macropodidae). I. The Petrogale assimilis species complex. G-banding and synaptonemal complex analysis. Cytogenet Cell Genet 48:228–232
Eldridge MDB, Johnston PG (1993) Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia: Macropodidae): VIII. An investigation of the nonrandom nature of karyotypic change. Genome 36:524–534
Eldridge MDB, Johnston PG, Close RL, Lowry PS (1989) Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia, Macropodidae).4. G-banding analysis of the Petrogale lateralis complex. Genome 32:935–940
Eldridge MDB, Johnston PG, Lowry PS (1992) Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia, Macropodidae).VII. G-banding analysis of Petrogale brachyotis and P. concinna. Cytogenet Cell Genet 60:34–39
Eldridge MDB, Metcalfe CJ (2006) Marsupialia. In: O’Brien SJ, Menninger JC, Nash WG (eds) Atlas mammalian chromosomes. Wiley, pp 9–62
Eldridge MDB, Pearson DJ (1997) Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia: Macropodidae). IX. Further G-banding studies of the Petrogale lateralis complex: P. lateralis pearsoni, the West Kimberley race, and a population heterozygous for a centric fusion. Genome 40:84–90. doi:10.1139/g97-011
Farré M, Robinson TJ, Ruiz-Herrera A (2015) An integrative breakage model of genome architecture, reshuffling and evolution: the integrative breakage model of genome evolution, a novel multidisciplinary hypothesis for the study of genome plasticity. BioEssays 37:479–488. doi:10.1002/bies.201400174
Gandhi MJ, Strong DM (2007) Donor derived malignancy following transplantation: a review. Cell Tissue Bank 8:267–286. doi:10.1007/s10561-007-9036-1
Glas R, De Leo AA, Delbridge ML et al (1999) Chromosome painting in marsupials: Genome conservation in the kangaroo family. Chromosom Res 7:167–176. doi:10.1023/A:1009291030968
Goodstadt L, Heger A, Webber C, Ponting CP (2007) An analysis of the gene complement of a marsupial, Monodelphis domestica: evolution of lineage-specific genes and giant chromosomes. Genome Res 17:969–981. doi:10.1101/gr.6093907
Griffin DK, Robertson LBW, Tempest HG, Skinner BM (2007) The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenet Genome Res 117:64–77. doi:10.1159/000103166
Griner LA (1979) Neoplasms in Tasmanian devils (Sarcophilus harrisii). J Natl Cancer Inst 62:589–595. doi:10.1093/jnci/62.3.589
Harley CB, Futcher AB, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345:458–60. doi:10.1038/345458a0
Hawkins CE, Baars C, Hesterman H et al (2006) Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii. Biol Conserv 131:307–324. doi:10.1016/j.biocon.2006.04.010
Hayman D (1989) Marsupial cytogenetics. Aust J Zool 37:331. doi:10.1071/ZO9890331
Hayman DL, Martin PG (1974) Mammalia I: Monotremata and Marsupialia. Anim. Cytogenet. vol 4 Chordata
Ingles ED, Deakin JE (2015) Global DNA methylation patterns on marsupial and devil facial tumour chromosomes. Mol Cytogenet 8:74. doi:10.1186/s13039-015-0176-x
Jordan HE (1911) The microscopic anatomy of the epiphysis of the opossum. Anat Rec 5:325–338. doi:10.1002/ar.1090050702
Kasai F, O’Brien PCM, Martin S, Ferguson-Smith MA (2012) Extensive homology of chicken macrochromosomes in the karyotypes of Trachemys scripta elegans and Crocodylus niloticus revealed by chromosome painting despite long divergence times. Cytogenet Genome Res 136:303–7. doi:10.1159/000338111
Kong CM, Lee XW, Wang X (2013) Telomere shortening in human diseases. FEBS J 280:3180–3193. doi:10.1111/febs.12326
Larkin DM, Pape G, Donthu R et al (2009) Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories. Genome Res 19:770–777. doi:10.1101/gr.086546.108
Loebel DA, Johnston PG (1993) Analysis of DNase 1 sensitivity and methylation of active and inactive X chromosomes of kangaroos (Macropus robustus) by in situ nick translation., pp 81–87
Longo MS, Carone DM, Program NCS et al (2009) Distinct retroelement classes define evolutionary breakpoints demarcating sites of evolutionary novelty. BMC Genomics 10:334. doi:10.1186/1471-2164-10-334
McCallum H, Jones M, Hawkins C et al (2009) Transmission dynamics of Tasmanian devil facial tumor disease may lead to disease-induced extinction. Ecology 90:3379–3392. doi:10.1890/08-1763.1
McClintock B (1941) The stability of broken ends of chromosomes in Zea mays. Genetics 26:234–282. doi:10.1038/378739a0
Metcalfe CJ, Eldridge MDB, McQuade LR, Johnston PG (1997) Mapping the distribution of the telomeric sequence (T2AG3) n in rock-wallabies, Petrogale (Marsupialia: Macropodidae), by fluorescence in situ hybridization. I. The penicillata complex. Cytogenet Genome Res 78:74–80. doi:10.1159/000134634
Metcalfe CJ, Eldridge MDB, Toder R, Johnston PG (1998) Mapping the distribution of the telomeric sequence (T2AG3)n in the Macropodoidea (Marsupialia), by fluorescence in situ hybridization. I. The swamp wallaby, Wallabia bicolor. Chromosom Res 6:603–610. doi:10.1023/A:1009249325574
Metcalfe CJ, Eldridge MDB, Johnston PG (2002) Mapping the distribution of the telomeric sequence (T2AG3)n in rock wallabies, Petrogale (Marsupialia: Macropodidae), by fluorescence in situ hybridization II. The lateralis complex. Cytogenet Genome Res 96:169–175. doi:10.1159/000063037
Metcalfe CJ, Eldridge MDB, Johnston PG (2004) Mapping the distribution of the telomeric sequence (T2AG3)n in the Macropodoidea (Marsupialia) by fluorescence in situ hybridization. II. The ancestral 2n = 22 macropodid karyotype. Cytogenet Genome Res 116:212–217. doi:10.1159/000098189
Metcalfe CJ, Bulazel KV, Ferreri GC et al (2007) Genomic instability within centromeres of interspecific marsupial hybrids. Genetics 177:2507–2517. doi:10.1534/genetics.107.082313
Metzger MJ, Reinisch C, Sherry J, Goff SP (2015) Horizontal transmission of clonal cancer cells causes leukemia in soft-shell clams. Cell 161:255–263. doi:10.1016/j.cell.2015.02.042
Miller W, Hayes VM, Ratan A et al (2011) Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil). Proc Natl Acad Sci U S A 108:12348–12353. doi:10.1073/pnas.1102838108
Murchison EP, Schulz-Trieglaff OB, Ning Z, et al. (2012) Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer. Cell 148:780–791. doi:10.1016/j.cell.2011.11.065
Murchison EP, Tovar C, Hsu A et al (2010) The Tasmanian devil transcriptome reveals Schwann cell origins of a clonally transmissible cancer. Science 327:84–87. doi:10.1126/science.1180616
Murphy WJ, Larkin DM, Everts-van der Wind A et al (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309:613–617. doi:10.1126/science.1111387
Nadeau JH, Taylor BA (1984) Lengths of chromosomal segments conserved since divergence of man and mouse. Proc Natl Acad Sci U S A 81:814–818. doi:10.1073/pnas.81.3.814
O’Neill RJ, O’Neill MJ, Graves JA (1998) Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393:68–72. doi:10.1038/nature01162
O’Neill RJW, Eldridge MDB, Toder R et al (1999) Chromosome evolution in kangaroos (Marsupialia: Macropodidae): cross species chromosome painting between the tammar wallaby and rock wallaby spp. with the 2n = 22 ancestral macropodid karyotype. Genome 42:525–30. doi:10.1139/g98-159
O’Neill RJW, Eldridge MDB, Graves JAM (2001) Chromosome heterozygosity and de novo chromosome rearrangements in mammalian interspecies hybrids. Mamm Genome 12:256–259. doi:10.1007/s003350010270
Painter TS (1922) Studies in mammalian spermatogenesis. I. The spermatogenesis of the opossum. J Exp Zool 35:13–45. doi:10.1002/jez.1400350103
Pearse A-M, Swift K (2006) Allograft theory: transmission of devil facial-tumour disease. Nature 439:549. doi:10.1038/439549a
Pearse A-M, Swift K, Hodson P et al (2012) Evolution in a transmissible cancer: a study of the chromosomal changes in devil facial tumor (DFT) as it spreads through the wild Tasmanian devil population. Cancer Genet 205:101–12. doi:10.1016/j.cancergen.2011.12.001
Peng Q, Pevzner PA, Tesler G (2006) The fragile breakage versus random breakage models of chromosome evolution. PLoS Comput Biol 2:100–111. doi:10.1016/j.jallcom.2005.07.024
Pevzner P, Tesler G (2003) Genome rearrangements in mammalian evolution: lessons from human and mouse genomes. Genome Res 13:37–45. doi:10.1101/gr.757503
Potter S, Moritz C, Eldridge MDB (2015) Gene flow despite complex Robertsonian fusions among rock-wallaby (Petrogale) species. Biol Lett. doi:10.1098/rsbl.2015.0731
Putnam NH, Connell BO, Stites JC et al (2016) Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res 26:342–350. doi:10.1101/gr.193474.115.Freely
Pye RJ, Pemberton D, Tovar C et al (2016) A second transmissible cancer in Tasmanian devils. Proc Natl Acad Sci 113:374–379. doi:10.1073/pnas.1519691113
Pyecroft SB, Pearse AM, Loh R et al (2007) Towards a case definition for devil facial tumour disease: what is it? Ecohealth 4:346–351. doi:10.1007/s10393-007-0126-0
Renfree MB, Papenfuss AT, Deakin JE et al (2011) Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. Genome Biol 12:R81. doi:10.1186/gb-2011-12-8-r81
Rens W, O’Brien PCM, Fairclough H et al (2003) Reversal and convergence in marsupial chromosome evolution. Cytogenet Genome Res 102:282–290. doi:10.1159/000075764
Rens W, O’Brien PCM, Yang F et al (1999) Karyotype relationships between four distantly related marsupials revealed by reciprocal chromosome painting. Chromosom Res 7:461–474. doi:10.1023/A:1009249813617
Rens W, Wallduck MS, Lovell FL et al (2010) Epigenetic modifications on X chromosomes in marsupial and monotreme mammals and implications for evolution of dosage compensation. Proc Natl Acad Sci U S A 107:17657–62. doi:10.1073/pnas.0910322107
Rofe R (1978) G-banded chromosomes and the evolution of Macropodidae. Aust Mammal 2:53–63
Rofe R, Hayman D (1985) G-banding evidence for a conserved complement in Marsupialia. Cytogenet Cell Genet 39:40–50
Ruiz-Herrera A, Castresana J, Robinson TJ (2006) Is mammalian chromosomal evolution driven by regions of genome fragility? Genome Biol 7:R115. doi:10.1186/gb-2006-7-12-r115
Ruiz-Herrera A, Robinson TJ (2008) Evolutionary plasticity and cancer breakpoints in human chromosome 3. BioEssays 30:1126–1137. doi:10.1002/bies.20829
Sharman G (1961) The mitotic chromosomes of marsupials and their bearing on taxonomy and phylogeny. Aust J Zool 9:38–60. doi:10.1071/ZO9610038
Sharman G, Close R, Maynes G (1989) Chromosome evolution, phylogeny and speciation of rock wallabies (Petrogale, Macropodidae). Aust J Zool 37:351. doi:10.1071/ZO9890351
Sharman GB, Close RL, Maynes GM (1990) Chromosome evolution, phylogeny and speciation of rock wallabies (Petrogale: Macropodidae). Aust J Zool 37:351–363
Shay JW, Bacchetti S (1997) A survey of telomerase activity in human cancer. Eur J Cancer 33:787–791. doi:10.1016/s0959-8049(97)00062-2
Siddle HV, Kreiss A, Eldridge MDB et al (2007) Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc Natl Acad Sci U S A 104:16221–16226. doi:10.1073/pnas.0704580104
Skinner BM, Griffin DK (2012) Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to breakpoints. Heredity (Edinb) 108:37–41. doi:10.1038/hdy.2011.99
Toder R, O’Neill RJW, Wienberg J et al (1997) Comparative chromosome painting between two marsupials: origins of an XX/XY1Y2 sex chromosome system. Mamm Genome 8:418–422. doi:10.1007/s003359900459
Tolar J, Neglia JP (2003) Transplacental and other routes of cancer transmission between individuals. J Pediatr Hematol Off J Am Soc Pediatr Hematol 25:430–434. doi:10.1097/00043426-200306000-00002
Tovar C, Obendorf D, Murchison EP et al (2011) Tumor-specific diagnostic marker for transmissible facial tumors of Tasmanian devils: immunohistochemistry studies. Vet Pathol 48:1195–203. doi:10.1177/0300985811400447
Ujvari B, Gatenby RA, Thomas F (2016) The evolutionary ecology of transmissible cancers. Infect Genet Evol 39:293–303. doi:10.1016/j.meegid.2016.02.005
Ujvari B, Pearse A-M, Peck S et al (2013) Evolution of a contagious cancer: epigenetic variation in Devil Facial Tumour Disease. Proc Biol Sci 280:20121720. doi:10.1098/rspb.2012.1720
Ujvari B, Pearse AM, Taylor R et al (2012) Telomere dynamics and homeostasis in a transmissible cancer. PLoS One 7:1–8. doi:10.1371/journal.pone.0044085
Volker M, Backstrom N, Skinner BM et al (2010) Copy number variation, chromosome rearrangement, and their association with recombination during avian evolution. Genome Res 20:503–511. doi:10.1101/gr.103663.109
Wang C, Deakin JE, Rens W et al (2011) A first-generation integrated tammar wallaby map and its use in creating a tammar wallaby first-generation virtual genome map. BMC Genomics 12:422. doi:10.1186/1471-2164-12-422
Welsh JS (2011) Contagious cancer. Oncologist 16:1–4. doi:10.1634/theoncologist.2010-0301
Westerman M, Woolley PA (1990) Cytogenetics of some New Guinean dasyurids and genome evolution in the Dasyuridae (Marsupialia). Aust J Zool 37:521–531. doi:10.1071/ZO9890521
Westerman M, Woolley PA (1993) Chromosomes and the evolution of dasyurid marsupials: an overview. Sci New Guinea 19:123–130
Young GJ, Graves JAM, Barbieri I, Woolley PA, Cooper DW (1982) The chromosomes of dasyurids (Masupialia). In: Archer M (ed) Carnivorous Marsupials. Royal Zoological Society, NSW., pp 783–795
Zhao H, Bourque G (2009) Recovering genome rearrangements in the mammalian phylogeny. Genome Res 19:934–942. doi:10.1101/gr.086009.108
Acknowledgments
We thank our collaborators A. Pearse, K. Swift and G. Woods who have provided chromosome preparations for our work on devils and devil facial tumour disease.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
JED has been supported by an Australian Research Council Future Fellowship (FT100100241) for work on Tasmanian devil and devil facial tumour chromosomes. An Australian Research Council Discovery Project (DP160100187) awarded to JED, Jason Bragg, Craig Moritz, Mark Eldridge and Mark Kirkpatrick is supporting our current work on chromosomal speciation in rock-wallabies.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 83 kb)
Rights and permissions
About this article
Cite this article
Deakin, J.E., Kruger-Andrzejewska, M. Marsupials as models for understanding the role of chromosome rearrangements in evolution and disease. Chromosoma 125, 633–644 (2016). https://doi.org/10.1007/s00412-016-0603-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-016-0603-8