Genomic correlates of recombination rate and its variability across eight recombination maps in the western honey bee (Apis mellifera L.)

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Ross, Caitlin R ^a   DeFelice, Dominick S ^a   Hunt, Greg J ^b   Ihle, Kate E ^c   Amdam, Gro V ^c,d   Rueppell, Olav ^a  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

^b PURDUE UNIVERSITY   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

^d NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Comparative genomics; GC content; Genome evolution; Hotspots; Meiotic recombination; Red queen hypothesis; Sociality

Indexed keywords

APIS MELLIFERA; ARTICLE; DNA BASE COMPOSITION; DNA STRUCTURE; GENE MAPPING; GENETIC LINKAGE; GENETIC RECOMBINATION; INSECT GENOME; MICROSATELLITE MARKER; NONHUMAN; NUCLEOTIDE MOTIF; ANIMAL; BEE; CHROMOSOME; CHROMOSOME MAP; CHROMOSOME SEGREGATION; GENETICS; MEIOSIS; MOLECULAR EVOLUTION;

APIS MELLIFERA; METAZOA;

ANIMALS; BASE COMPOSITION; BEES; CHROMOSOME MAPPING; CHROMOSOME SEGREGATION; CHROMOSOMES; EVOLUTION, MOLECULAR; GENOME, INSECT; MEIOSIS; RECOMBINATION, GENETIC;

EID: 84924342258     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1281-2     Document Type: Article

References (46)

1. de Massy B. Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu Rev Genet. 2013;47:563-99.
2. Borodin PM, Karamysheva TV, Belonogova NM, Torgasheva AA, Rubtsov NB, Searle JB. Recombination map of the common shrew, Sorex araneus (Eulipotyphla, Mammalia). Genetics. 2008;178(2):621-32.
3. Segura J, Ferretti L, Ramos-Onsins S, Capilla L, Farre M, Reis F, et al. Evolution of recombination in eutherian mammals: insights into mechanisms that affect recombination rates and crossover interference. Proc Biol Sci. 2013;280(1771):20131945.
4. Roeder GS. Meiotic chromosomes: it takes two to tango. Genes Dev. 1997;11(20):2600-21.
5. Lynch M. The origins of eukaryotic gene structure. Mol Biol Evol. 2006;23(2):450-68.
6. Dumont BL, Payseur BA. Evolution of the genomic rate of recombination in mammals. Evolution. 2008;62(2):276-94.
7. Comeron JM, Ratnappan R, Bailin S. The many landscapes of recombination in Drosophila melanogaster. PLoS Genet. 2012;8(10):e1002905.
8. Coop G, Wen XQ, Ober C, Pritchard JK, Przeworski M. High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science. 2008;319(5868):1395-8.
9. Beye M, Gattermeier I, Hasselmann M, Gempe T, Schioett M, Baines JF, et al. Exceptionally high levels of recombination across the honey bee genome. Genome Res. 2006;16(11):1339-44.
10. Meznar ER, Gadau J, Koeniger N, Rueppell O. Comparative linkage mapping suggests a high recombination rate in all honey bees. J Hered. 2010;101:S118-26.
11. Solignac M, Mougel F, Vautrin D, Monnerot M, Cornuet JM. A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol. 2007;8(4):R66.
12. Wilfert L, Gadau J, Schmid-Hempel P. Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity. 2007;98(4):189-97.
13. Sirvio A, Johnston JS, Wenseleers T, Pamilo P. A high recombination rate in eusocial Hymenoptera: evidence from the common wasp Vespula vulgaris. BMC Genet. 2011;12:95.
14. Gadau J, Page RE, Werren JH, Schmid-Hempel P. Genome organization and social evolution in hymenoptera. Naturwissenschaften. 2000;87(2):87-9.
15. Sirvio A, Gadau J, Rueppell O, Lamatsch D, Boomsma JJ, Pamilo P, et al. High recombination frequency creates genotypic diversity in colonies of the leaf-cutting ant Acromyrmex echinatior. J Evol Biol. 2006;19(5):1475-85.
16. Rueppell O, Meier S, Deutsch R. Multiple mating but not recombination causes quantitative increase in offspring genetic diversity for varying genetic architectures. PLoS One. 2012;7(10):e47220.
17. Sherman PW. Insect chromosome numbers and eusociality. Am Nat. 1979;113:925-35.
18. Templeton AR. Chromosome number, quantitative genetics and eusociality. Am Nat. 1979;113(6):937-41.
19. Kent CF, Zayed A. Evolution of recombination and genome structure in eusocial insects. Commun Integr Biol. 2013;6(2):e22919.
20. Weinstock GM, Robinson GE, Gibbs RA, Worley KC, Evans JD, Maleszka R, et al. Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 2006;443(7114):931-49.
21. Elsik CG, Worley KC, Bennett AK, Beye M, Camara F, Childers CP, et al. Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genomics. 2014;15(1):86.
22. Adrian AB, Comeron JM. The Drosophila early ovarian transcriptome provides insight to the molecular causes of recombination rate variation across genomes. BMC Genomics. 2013;14:794.
23. Wahls WP, Davidson MK. New paradigms for conserved, multifactorial, cis-acting regulation of meiotic recombination. Nucleic Acids Res. 2012;40(20):9983-9.
24. Berg IL, Neumann R, Lam KW, Sarbajna S, Odenthal-Hesse L, May CA, et al. PRDM9 variation strongly influences recombination hot-spot activity and meiotic instability in humans. Nat Genet. 2010;42(10):859-63.
25. Mougel F, Poursat MA, Beaume N, Vautrin D, Solignac M. High-resolution linkage map for two honeybee chromosomes: the hotspot quest. Mol Genet Genomics. 2014;289(1):11-24.
26. Bessoltane N, Toffano-Nioche C, Solignac M, Mougel F. Fine scale analysis of crossover and non-crossover and detection of recombination sequence motifs in the honeybee (Apis mellifera). PLoS One. 2012;7(5):e36229.
27. Ubeda F, Wilkins JF. The Red Queen theory of recombination hotspots. J Evol Biol. 2011;24(3):541-53.
28. Whitfield CW, Behura SK, Berlocher SH, Clark AG, Johnston JS, Sheppard WS, et al. Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science. 2006;314:642-5.
29. Ross C, DeFelice D, Hunt GJ, Ihle K, Rueppell O. A comparison of multiple genome-wide recombination maps in Apis mellifera. Topics from the 8th Annual UNCG Regional Mathematics and Statistics Conference 2014: in press.
30. Arechavaleta-Velasco ME, Alcala-Escamilla K, Robles-Rios C, Tsuruda JM, Hunt GJ. Fine-scale linkage mapping reveals a small set of candidate genes influencing honey bee grooming behavior in response to Varroa mites. PLoS One. 2012;7(11):e47269.
31. Tsuruda JM, Harris JW, Bourgeois L, Danka RG, Hunt GJ. High-resolution linkage analyses to identify genes that influence Varroa Sensitive Hygiene behavior in honey bees. PLoS One. 2012;7(11):e48276.
32. Ball AD, Stapley J, Dawson DA, Birkhead TR, Burke T, Slate J. A comparison of SNPs and microsatellites as linkage mapping markers: lessons from the zebra finch (Taeniopygia guttata). BMC Genomics. 2010;11:218. doi:10.1186/1471-2164-11-218.
33. Kennedy GC, Matsuzaki H, Dong S, Liu WM, Huang J, Liu G, et al. Large-scale genotyping of complex DNA. Nat Biotechnol. 2003;21:1233-7.
34. Pessia E, Popa A, Mousset S, Rezvoy C, Duret L, Marais GA. Evidence for widespread GC-biased gene conversion in eukaryotes. Genome Biol Evol. 2012;4(7):675-82.
35. Robinson MC, Stone EA, Singh ND. Population genomic analysis reveals no evidence for gc-biased gene conversion in Drosophila melanogaster. Mol Biol Evol. 2014;31(2):425-33.
36. Kent CF, Minaei S, Harpur BA, Zayed A. Recombination is associated with the evolution of genome structure and worker behavior in honey bees. Proc Natl Acad Sci U S A. 2012;109(44):18012-7.
37. Nicolas A. Relationship between transcription and initiation of meiotic recombination: toward chromatin accessibility. Proc Natl Acad Sci U S A. 1998;95(1):87-9.
38. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, Tischfield SE, et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell. 2011;144(5):719-31.
39. Benet A, Molla G, Azorin F. d(GA x TC)(n) microsatellite DNA sequences enhance homologous DNA recombination in SV40 minichromosomes. Nucleic Acids Res. 2000;28(23):4617-22.
40. Illingworth CJR, Parts L, Bergström A, Liti G, Mustonen V. Inferring genome-wide recombination landscapes from advanced intercross lines: application to yeast crosses. PLoS One. 2013;8(5):e62266.
41. Heil CSS, Noor MAF. Zinc finger binding motifs do not explain recombination rate variation within or between species of Drosophila. PLoS One. 2012;7(9):e45055.
42. Page RE, Fondrk MK. The effects of colony level selection on the social organization of honey bee (Apis mellifera L) colonies - colony level components of pollen hoarding. Behav Ecol Sociobiol. 1995;36(2):135-44.
43. Ihle KE, Rueppell O, Page RE, Amdam GV. QTL for ovary size and juvenile hormone response to Vg-RNAi knockdown. J Hered. 2015: online: doi:10.1093/jhered/esu086.
44. Rueppell O, Metheny JD, Linksvayer TA, Fondrk MK, Page Jr RE, Amdam GV. Genetic architecture of ovary size and asymmetry in European honeybee workers. Heredity. 2011;106:894-903.
45. Graham AM, Munday MD, Kaftanoglu O, Page Jr RE, Amdam GV, Rueppell O. Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.). BMC Evol Biol. 2011;11:95.
46. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Res. 2008;36:W5-9.