Skip to main content

Marsupial Linkage Maps

  • Chapter
  • First Online:
Marsupial Genetics and Genomics

Abstract

Linkage maps provide information not only on the linear order of genetic loci on chromosomes; they also reveal the locations and frequencies of crossover events during gametogenesis. As such they have been invaluable resources for genetic mapping for nearly 100 years and continue to be extremely useful for providing insight into the meiotic process and disruptions thereof that physical mapping strategies cannot furnish. Linkage mapping research with marsupial mammals had a late inception due to a long-standing lack of animal resources amenable to the reliable, multigenerational breeding programs necessary for the establishment of genetic lines and tools required for linkage-mapping studies. As this impediment was overcome through the establishment of several self-perpetuating marsupial breeding colonies late in the twentieth century, linkage mapping studies began to uncover evidence of unexpectedly low rates and unusual sex-specific patterns of recombination that run counter to those observed for almost all other vertebrates examined. This chapter describes the history of linkage research in marsupials, summarizes the linkage maps of the tammar wallaby and the gray, short-tailed opossum, considers the value of these linkage maps in connection with the recent opossum and wallaby genome projects, and discusses the extent and implications of low recombination rates and sex-specific recombination differences in these species. The chapter ends with speculation on the potential of the opossum as a model for recombination research.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Akesson M, Hansson B, Hasselquist D, Bensch S (2007) Linkage mapping of AFLP markers in a wild population of great reed warblers: importance of heterozygosity and number of genotyped individuals. Mol Ecol 16:2189–2202.

    Article  PubMed  Google Scholar 

  • Backstrom N, Karaiskou N, Leder EH, et al. (2008) A gene-based genetic linkage map of the collared flycatcher (Ficedula albicollis) reveals extensive synteny and gene-order conservation during 100 million years of avian evolution. Genetics 179:1479–1495.

    Article  PubMed  Google Scholar 

  • Barton NH, Otto SP (2005) Evolution of recombination due to random drift. Genetics 169:2353–2370.

    Article  PubMed  CAS  Google Scholar 

  • Bennett JH, Hayman DL, Hope RM (1986) Novel sex differences in linkage values and meiotic chromosome behaviour in a marsupial. Nature 323:59–60.

    Article  PubMed  CAS  Google Scholar 

  • Broman KW, Murray JC, Sheffield VC, White RL, Weber JL (1998) Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am J Hum Genet 63:861–869.

    Article  PubMed  CAS  Google Scholar 

  • Buard J, de Massy B (2007) Playing hide and seek with mammalian meiotic crossover hotspots. Trends Genet 23:301–309.

    Article  PubMed  CAS  Google Scholar 

  • Calderon PL, Pigozzi MI (2006) MLH1-focus mapping in birds shows equal recombination between sexes and diversity of crossover patterns. Chromosome Res 14:605–612.

    Article  PubMed  CAS  Google Scholar 

  • Coop G, Przeworski M (2007) An evolutionary view of human recombination. Nat Rev Genet 8:23–34.

    Article  PubMed  CAS  Google Scholar 

  • Cooper DW, Johnston PG, VandeBerg JL, Robinson ES (1990) X-chromosome inactivation in marsupials. In: Graves JAM, Hope R, Cooper DW (eds) Mammals from Pouches and Eggs: Genetics, Breeding and Evolution of Marsupials and Monotremes. CSIRO, Melbourne.

    Google Scholar 

  • Cooper DW, Johnston PG, Watson JM, Graves JAM (1993) X-inactivation in marsupials and monotremes. Sem Dev Biol 4:117–128.

    Article  Google Scholar 

  • Cooper DW, VandeBerg JL, Sharman GB, Poole WE (1971) Phosphoglycerate kinase polymorphism in kangaroos provides further evidence for paternal X inactivation. Nat New Biol 230:155–157.

    Article  PubMed  CAS  Google Scholar 

  • de Visser JA, Elena SF (2007) The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet 8:139–149.

    Article  PubMed  Google Scholar 

  • Duke SE, Samollow PB, Mauceli E, Lindblad-Toh K, Breen M (2007) Integrated cytogenetic BAC map of the genome of the gray, short-tailed opossum, Monodelphis domestica. Chromosome Res 15:361–370.

    PubMed  CAS  Google Scholar 

  • Dumont BL, Payseur BA (2008) Evolution of the genomic rate of recombination in mammals. Evolution 62:276–294.

    Article  PubMed  CAS  Google Scholar 

  • Duret L, Eyre-Walker A, Galtier N (2006) A new perspective on isochore evolution. Gene 385:71–74.

    Article  PubMed  CAS  Google Scholar 

  • Galtier N, Piganeau G, Mouchiroud D, Duret L (2001) GC-content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics 159:907–911.

    PubMed  CAS  Google Scholar 

  • Gandon S, Otto SP (2007) The evolution of sex and recombination in response to abiotic or coevolutionary fluctuations in epistasis. Genetics 175:1835–1853.

    Article  PubMed  CAS  Google Scholar 

  • Graves JA, Westerman M (2002) Marsupial genetics and genomics. Trends Genet 18:517–521.

    Article  PubMed  Google Scholar 

  • Groenen MA, Wahlberg P, Foglio M, et al. (2009) A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Res 19:510–519.

    Article  PubMed  CAS  Google Scholar 

  • Hayman D, Moore H, Evans E (1988) Further evidence of novel sex differences in chiasma distribution in marsupials. Heredity 61:455–458.

    Article  Google Scholar 

  • Hayman DL, Rodger JC (1990) Meiosis in male and female Trichosurus vulpecula (Marsupialia). Heredity 64:251–254.

    Article  Google Scholar 

  • Hayman DL, Smith MJ, Rodger JC (1990) A comparative study of chiasmata in male and female Bettongia penicillata (Marsupialia). Genetica 83:45–49.

    Google Scholar 

  • Hedrick PW (2007) Sex: differences in mutation, recombination, selection, gene flow, and genetic drift. Evolution 61:2750–2771.

    Article  PubMed  Google Scholar 

  • Hinds LA, Poole WE, Tyndale-Biscoe CH, van Oorschot RAH, Cooper DW (1990) Reproductive biology and the potential for genetic studies in the tammar wallaby, Macropus eugenii. Aust J Zool 37:223–234.

    Article  Google Scholar 

  • Hogstrand K, Bohme J (1999) Gene conversion of major histocompatibility complex genes is associated with CpG-rich regions. Immunogenetics 49:446–455.

    Article  PubMed  CAS  Google Scholar 

  • Hope RM (1993) Selected features of marsupial genetics. Genetica 90:165–180.

    Article  PubMed  CAS  Google Scholar 

  • Hunt PA (2006) Meiosis in mammals: recombination, non-disjunction and the environment. Biochem Soc Trans 34:574–577.

    Article  PubMed  CAS  Google Scholar 

  • Ivanovska I, Orr-Weaver TL (2006) Histone modifications and the chromatin scaffold for meiotic chromosome architecture. Cell Cycle 5:2064–2071.

    Article  PubMed  CAS  Google Scholar 

  • Jaari S, Li MH, Merila J (2009) A first-generation microsatellite-based genetic linkage map of the Siberian jay (Perisoreus infaustus): insights into avian genome evolution. BMC Genomics 10:1.

    Article  PubMed  Google Scholar 

  • Kai W, Kikuchi K, Fujita M, et al. (2005) A genetic linkage map for the tiger pufferfish, Takifugu rubripes. Genetics 171:227–238.

    Article  PubMed  CAS  Google Scholar 

  • Kauppi L, Jeffreys AJ, Keeney S (2004) Where the crossovers are: recombination distributions in mammals. Nat Rev Genet 5:413–424.

    Article  PubMed  CAS  Google Scholar 

  • Kochakpour N, Moens PB (2008) Sex-specific crossover patterns in Zebrafish (Danio rerio). Heredity 100:489–495.

    Article  PubMed  CAS  Google Scholar 

  • Kong A, Gudbjartsson DF, Sainz J, et al. (2002) A high-resolution recombination map of the human genome. Nat Genet 31:241–247.

    PubMed  CAS  Google Scholar 

  • Kucuktas H, Wang S, Li P, et al. (2009) Construction of genetic linkage maps and comparative genome analysis of catfish using gene-associated markers. Genetics 181:1649–1660.

    Article  PubMed  CAS  Google Scholar 

  • Lenormand T (2003) The evolution of sex dimorphism in recombination. Genetics 163:811–822.

    PubMed  Google Scholar 

  • Lenormand T, Dutheil J (2005) Recombination difference between sexes: a role for haploid selection. PLoS Biol 3:e63.

    Article  PubMed  Google Scholar 

  • Lercher MJ, Hurst LD (2003) Imprinted chromosomal regions of the human genome have unusually high recombination rates. Genetics 165:1629–1632.

    PubMed  CAS  Google Scholar 

  • Liao W, Collins A, Hobbs M, Khatkar MS, Luo J, Nicholas FW (2007) A comparative location database (CompLDB): map integration within and between species. Mamm Genome 18:287–299.

    Article  PubMed  CAS  Google Scholar 

  • Maddox JF, Davies KP, Crawford AM, et al. (2001) An enhanced linkage map of the sheep genome comprising more than 1000 loci. Genome Res 11:1275–1289.

    Article  PubMed  CAS  Google Scholar 

  • Martin G, Otto SP, Lenormand T (2006) Selection for recombination in structured populations. Genetics 172:593–609.

    Article  PubMed  CAS  Google Scholar 

  • Matise TC, Chen F, Chen W, et al. (2007) A second-generation combined linkage physical map of the human genome. Genome Res 17:1783–1786.

    Article  PubMed  CAS  Google Scholar 

  • McKenzie LM, Collet C, Cooper DW (1993) Use of a subspecies cross for efficient development of a linkage map for a marsupial mammal, the tammar wallaby (Macropus eugenii). Cytogenet Cell Genet 64:264–267.

    Article  PubMed  CAS  Google Scholar 

  • McKenzie LM, Johnston PG, Eldridge MD, Cooper DW (1996) Close linkage between RNR and GPD genes on the tammar wallaby (Macropus eugenii) X chromosome. Cytogenet Cell Genet 72:197–199.

    Article  PubMed  CAS  Google Scholar 

  • Menotti-Raymond M, David VA, Schaffer AA, et al. (2009) An autosomal genetic linkage map of the domestic cat, Felis silvestris catus. Genomics 93:305–313.

    Article  PubMed  CAS  Google Scholar 

  • Mikkelsen TS, Wakefield MJ, Aken B, et al. (2007) Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences. Nature 447:167–177.

    Article  PubMed  CAS  Google Scholar 

  • Moen T, Hayes B, Baranski M, et al. (2008) A linkage map of the Atlantic salmon (Salmo salar) based on EST-derived SNP markers. BMC Genomics 9:223.

    Article  PubMed  Google Scholar 

  • Moens PB, Marcon E, Shore JS, Kochakpour N, Spyropoulos B (2007) Initiation and resolution of interhomolog connections: crossover and non-crossover sites along mouse synaptonemal complexes. J Cell Sci 120:1017–1027.

    Article  PubMed  CAS  Google Scholar 

  • Morelli MA, Cohen PE (2005) Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130:761–781.

    Article  PubMed  CAS  Google Scholar 

  • Morgan TH (1911a). Random segregation versus coupling in Mendelian inheritance. Science 34:384.

    Article  PubMed  CAS  Google Scholar 

  • Morgan TH (1911b). Chromosomes and associative inheritance. Science 34:636–638.

    Article  PubMed  CAS  Google Scholar 

  • Morgan TH (1911c). An attempt to analyze the constitution of the chromosomes on the basis of sex-limited inheritance in Drosophila. J Exp Zool 11:365–413.

    Article  Google Scholar 

  • Ng SH, Madeira R, Parvanov ED, Petros LM, Petkov PM, Paigen K (2009) Parental origin of chromosomes influences crossover activity within the Kcnq1 transcriptionally imprinted domain of Mus musculus. BMC Mol Biol 10:43.

    Article  PubMed  Google Scholar 

  • Ohno S (1967) Sex-Chromosomes and Sex-Linked Genes. Springer, Berlin.

    Book  Google Scholar 

  • Otto SP, Gerstein AC (2006) Why have sex? The population genetics of sex and recombination. Biochem Soc Trans 34:519–522.

    Article  PubMed  CAS  Google Scholar 

  • Otto SP, Lenormand T (2002) Resolving the paradox of sex and recombination. Nat Rev Genet 3:252–261.

    Article  PubMed  CAS  Google Scholar 

  • Perelygin AA, Samollow PB, Perelygina LM, Cherry LM, Mahaney SM, VandeBerg JL (1996) A new DNA marker, U15557, is linked to protease inhibitor and adenylate kinase-1 in the laboratory opossum, Monodelphis domestica. Anim Genet 27:113–116.

    Article  PubMed  CAS  Google Scholar 

  • Petkov PM, Broman KW, Szatkiewicz JP, Paigen K (2007) Crossover interference underlies sex differences in recombination rates. Trend Genet 23:539–542.

    Article  CAS  Google Scholar 

  • Petronczki M, Siomos MF, Nasmyth K (2003) Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–440.

    Article  PubMed  CAS  Google Scholar 

  • Reid DP, Smith CA, Rommens M, Blanchard B, Martin-Robichaud D, Reith M (2007) A genetic linkage map of Atlantic halibut (Hippoglossus hippoglossus L.). Genetics 177:1193–1205.

    Article  PubMed  CAS  Google Scholar 

  • Rice WR (2002) Experimental tests of the adaptive significance of sexual recombination. Nat Rev Genet 3:241–251.

    Article  PubMed  CAS  Google Scholar 

  • Richardson BJ, Czuppon AB, Sharman GB (1971) Inheritance of glucose-6-phosphate dehydrogenase variation in kangaroos. Nat New Biol 230:154–155.

    PubMed  CAS  Google Scholar 

  • Samollow PB, Gouin N, Miethke P, et al. (2007) A microsatellite-based, physically anchored linkage map for the gray, short-tailed opossum (Monodelphis domestica). Chromosome Res 15:269–281.

    PubMed  CAS  Google Scholar 

  • Samollow PB, Graves JAM (1998) Gene maps of marsupials. ILAR J 39:203–224.

    PubMed  Google Scholar 

  • Samollow PB, Kammerer CM, Mahaney SM, et al. (2004) First generation linkage map of the gray, short-tailed opossum, Monodelphis domestica, reveals genome-wide reduction in female recombination rates. Genetics 166:307–329.

    Article  PubMed  CAS  Google Scholar 

  • Sandovici I, Kassovska-Bratinova S, Vaughan JE, Stewart R, Leppert M, Sapienza C (2006) Human imprinted chromosomal regions are historical hot-spots of recombination. PLoS Genet 2:e101.

    Article  PubMed  Google Scholar 

  • Shifman S, Bell JT, Copley RR, et al. (2006) A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biol 4:e395.

    Article  PubMed  Google Scholar 

  • Sigurdsson MI, Smith AV, Bjornsson HT, Jonsson JJ (2009) HapMap methylation-associated SNPs, markers of germline DNA methylation, positively correlate with regional levels of human meiotic recombination. Genome Res 19:581–589.

    Article  PubMed  CAS  Google Scholar 

  • Singer A, Perlman H, Yan Y, et al. (2002) Sex-specific recombination rates in zebrafish (Danio rerio). Genetics 160:649–657.

    PubMed  CAS  Google Scholar 

  • Stapley J, Birkhead TR, Burke T, Slate J (2008) A linkage map of the zebra finch Taeniopygia guttata provides new insights into avian genome evolution. Genetics 179:651–667.

    Article  PubMed  CAS  Google Scholar 

  • Sturtevant AH (1913) The linear arrangement of six sex-linked factors in Drosophila, as shown by their mode of inheritance. J Exp Zool 14:43–59.

    Article  Google Scholar 

  • VandeBerg JL (1990) The gray, short-tailed opossum (Monodelphis domestica) as a model didelphid for genetic research. Aust J Zool 37:235–247.

    Article  Google Scholar 

  • VandeBerg JL, Robinson ES (1997) The laboratory opossum (Monodelphis domestica) in laboratory research. ILAR Journal 38:4–12.

    PubMed  Google Scholar 

  • VandeBerg JL, Robinson ES, Samollow PB, Johnston PG (1987) X-linked gene expression and X-chromosome inactivation: marsupials, mouse, and man compared. Isozymes Curr Top Biol Med Res 15:225–253.

    PubMed  CAS  Google Scholar 

  • van Oorschot RA, Birmingham V, Porter PA, Kammerer CM, VandeBerg JL (1993) Linkage between complement components 6 and 7 and glutamic pyruvate transaminase in the marsupial Monodelphis domestica. Biochem Genet 31:215–222.

    Article  PubMed  Google Scholar 

  • van Oorschot RAH, Cooper DW (1989) A conserved linkage between PI and GPI in a marsupial mammal, the tammar wallaby (Macropus eugenii). Cytogenet Cell Genet 51:1097.

    Google Scholar 

  • van Oorschot RA, Porter PA, Kammerer CM, VandeBerg JL (1992) Severely reduced recombination in females of the South American marsupial Monodelphis domestica. Cytogenet Cell Genet 60:64–67.

    Article  PubMed  Google Scholar 

  • Vingborg RK, Gregersen VR, Zhan B, et al. (2009) A robust linkage map of the porcine autosomes based on gene-associated SNPs. BMC Genomics 10:134.

    Article  PubMed  Google Scholar 

  • Warren WC, Hillier LW, Marshall Graves JA, et al. (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature 453:175–183.

    Article  PubMed  CAS  Google Scholar 

  • Zenger KR, McKenzie LM, Cooper DW (2002) The first comprehensive genetic linkage map of a marsupial: the tammar wallaby (Macropus eugenii). Genetics 162:321–330.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The author’s work is supported in part by grant RR014214 from the National Center for Research Resources of the National institutes of Health (USA).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul B. Samollow .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Samollow, P.B. (2010). Marsupial Linkage Maps. In: Deakin, J., Waters, P., Marshall Graves, J. (eds) Marsupial Genetics and Genomics. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9023-2_4

Download citation

Publish with us

Policies and ethics