Abstract
Meiotic recombination is an essential component of eukaryotic sexual reproduction, but its frequency varies within and between genomes. Although it is well established that honey bees have a high recombination rate with about 20 cM/Mbp, the proximate and ultimate causes of this exceptional rate are poorly understood. Here, we describe six linkage maps of the western honey bee Apis mellifera that were produced with consistent methodology from samples from distinct parts of the species near global distribution. We compared the genome-wide rates and distribution of meiotic crossovers among the six maps and found considerable differences. Overall similarity of local recombination rates among our samples was unrelated to geographic or phylogenetic distance of the populations that our samples were derived from. However, the limited sampling constrains the interpretation of our results, because it is unclear how representative these samples were. In contrast to previous studies, we found only in two datasets a significant relation between local recombination rate and GC content. Focusing on regions of particularly increased or decreased recombination in specific maps, we identified several enriched gene ontologies in these regions and speculated about their local adaptive relevance. These data are contributing to an increasing comparative effort to gain an understanding of the intra-specific variability of recombination rates and their evolutionary role in honey bees and other social insects.
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References
Alleman A, Feldmeyer B, Foitzik S (2018) Comparative analyses of co-evolving host-parasite associations reveal unique gene expression patterns underlying slavemaker raiding and host defensive phenotypes. Sci Rep 8:1951
Amdam GV, Norberg K, Omholt SW, Kryger P, Lourenco AP, Bitondi MMG, Simoes ZLP (2005) Higher vitellogenin concentrations in honey bee workers may be an adaptation to life in temperate climates. Insectes Soc 52:316–319
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300
Bessoltane N, Toffano-Nioche C, Solignac M, Mougel F (2012) Fine scale analysis of crossover and non-crossover and detection of recombination sequence motifs in the honeybee (Apis mellifera). PLoS One 7:e36229
Beye M et al (2006) Exceptionally high levels of recombination across the honey bee genome. Genome Res 16:1339–1344
Bourgeois AL, Rinderer TE (2009) Genetic characterization of Russian Honey Bee stock selected for improved resistance to Varroa destructor. J Econ Entomol 102:1233–1238
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140
Charlesworth B, Charlesworth D (1985) Genetic variation in recombination. I. Responses to selection and preliminary genetic analysis. Heredity 54:71–83
Comeron JM, Ratnappan R, Bailin S (2012) The many landscapes of recombination in Drosophila melanogaster. PLoS Genet 8:e1002905
Conlon B, Frey E, Rosenkranz P, Locke B, Moritz R, Routtu J (2018) The role of epistatic interactions underpinning resistance to parasitic Varroa mites in haploid honeybee drones. J Evol Biol 31:801–809
Coop G, Wen XQ, Ober C, Pritchard JK, Przeworski M (2008) High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science 319:1395–1398
Cvetković D, Tucić N (1986) Female recombination rates and fitness in Drosophila melanogaster. J Zool Syst Evol Res 24:198–207
De Villena FP-M, Sapienza C (2001) Recombination is proportional to the number of chromosome arms in mammals. Mamm Genome 12:318–322
Dumont BL, White MA, Steffy B, Wiltshire T, Payseur BA (2011) Extensive recombination rate variation in the house mouse species complex inferred from genetic linkage maps. Genome Res 21:114–125
Elsik C et al (2014) Finding the missing honey bee genes: lessons learned from a genome upgrade. BMC Genom 15:86
Elsik CG, Tayal A, Diesh CM, Unni DR, Emery ML, Nguyen HN, Hagen DE (2015) Hymenoptera Genome Database: integrating genome annotations in HymenopteraMine. Nucleic Acids Res 44:D793–D800
Feyereisen R (1999) Insect P450 enzymes. Annu Rev Entomol 44:507–533
Fledel-Alon A, Wilson DJ, Broman K, Wen X, Ober C, Coop G, Przeworski M (2009) Broad-scale recombination patterns underlying proper disjunction in humans. PLoS Genet 5:e1000658
Harpur BA, Minaei S, Kent CF, Zayed A (2012) Management increases genetic diversity of honey bees via admixture. Mol Ecol 21:4414–4421
Harpur BA, Kent CF, Molodtsova D, Lebon JM, Alqarni AS, Owayss AA, Zayed A (2014) Population genomics of the honey bee reveals strong signatures of positive selection on worker traits. Proc Natl Acad Sci 111:2614–2619
Hartfield M, Keightley PD (2012) Current hypotheses for the evolution of sex and recombination. Integr Zool 7:192–209
Hasegawa M et al (2009) Differential gene expression in the mandibular glands of queen and worker honeybees, Apis mellifera L.: implications for caste-selective aldehyde and fatty acid metabolism. Insect Biochem Mol 39:661–667
Hill WG, Robertson A (1966) The effect of linkage on limits to artificial selection. Genet Res 8:269–294
Hillers KJ (2004) Crossover interference. Curr Biol 14:R1036–R1037
Huang W et al (2014) Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines. Genome Res 24:1193–1208
Hunt GJ, Page RE (1995) Linkage map of the honey bee, Apis mellifera, based on RAPD markers. Genetics 139:1371–1382
Hunter CM, Huang W, Mackay TF, Singh ND (2016) The genetic architecture of natural variation in recombination rate in Drosophila melanogaster. PLoS Genet 12:e1005951
Johnston SE, Bérénos C, Slate J, Pemberton JM (2016) Conserved genetic architecture underlying individual recombination rate variation in a wild population of Soay sheep (Ovis aries). Genetics 203:583–598
Jones JC, Wallberg A, Christmas MJ, Kapheim KM, Webster MT (2019) Extreme differences in recombination rate between the genomes of a solitary and a social bee. Mol Biol Evol 36:2277–2291
Kapheim KM et al (2015) Genomic signatures of evolutionary transitions from solitary to group living. Science 348:1139–1143
Kavanagh K, Jörnvall H, Persson B, Oppermann U (2008) Medium- and short-chain dehydrogenase/reductase gene and protein families. Cell Mol Life Sci 65:3895
Kawakami T, Wallberg A, Olsson A, Wintermantel D, de Miranda JR, Allsopp M, Rundlӧf M, Webster MT (2019) Substantial heritable variation in recombination rate on multiple scales in honeybees and bumblebees. Genetics 212:1101–1119
Kent CF, Zayed A (2013) Evolution of recombination and genome structure in eusocial insects. Commun Integr Biol 6:e22919
Kent CF, Minaei S, Harpur BA, Zayed A (2012) Recombination is associated with the evolution of genome structure and worker behavior in honey bees. Proc Natl Acad Sci USA 109:18012–18017
Kocher SD et al (2013) The draft genome of a socially polymorphic halictid bee, Lasioglossum albipes. Genome Biol 14:R142
Kohl KP, Sekelsky J (2013) Meiotic and mitotic recombination in meiosis. Genetics 194:327–334
Kong A et al (2004) Recombination rate and reproductive success in humans. Nat Genet 36:1203
Langberg K, Phillips M, Rueppell O (2018) Testing the effect of paraquat exposure on genomic recombination rates in queens of the western honey bee, Apis mellifera. Genetica 146:171–178
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391
Lenormand T, Engelstädter J, Johnston SE, Wijnker E, Haag CR (2016) Evolutionary mysteries in meiosis. Philos Trans R Soc B 371:20160001
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760
Li H et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079
Liu H, Zhang X, Huang J, Chen J-Q, Tian D, Hurst L, Yang S (2015) Causes and consequences of crossing-over evidenced via a high-resolution recombinational landscape of the honey bee. Genome Biol 16:15
Lowell BB, Spiegelman BM (2000) Towards a molecular understanding of adaptive thermogenesis. Nature 404:652
Lynch M (2006) The origins of eukaryotic gene structure. Mol Biol Evol 23:450–468
Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364
Meixner MD, Costa C, Kryger P, Hatjina F, Bouga M, Ivanova E, Büchler R (2010) Conserving diversity and vitality for honey bee breeding. J Apic Res 49:85–92
Meixner MD, Büchler R, Costa C, Francis RM, Hatjina F, Kryger P, Uzunov A, Carreck NL (2014) Honey bee genotypes and the environment. J Apic Res 53:183–187
Mougel F, Poursat M-A, Beaume N, Vautrin D, Solignac M (2014) High-resolution linkage map for two honeybee chromosomes: the hotspot quest. Mol Genet Genom 289:11–24
Mugal CF, Weber CC, Ellegren H (2015) GC-biased gene conversion links the recombination landscape and demography to genomic base composition: GC-biased gene conversion drives genomic base composition across a wide range of species. BioEssays 37:1317–1326
Myers S, Bottolo L, Freeman C, McVean G, Donnelly P (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310:321–324
Otto SP, Barton NH (2001) Selection for recombination in small populations. Evolution 55:1921–1931
Pearson P, Ellis J, Evans H (1970) A gross reduction in chiasma formation during meiotic prophase and a defective DNA repair mechanism associated with a case of human male infertility. Cytogenet Genome Res 9:460–467
Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135
Pinto MA et al (2014) Genetic integrity of the Dark European honey bee (Apis mellifera mellifera) from protected populations: a genome-wide assessment using SNPs and mtDNA sequence data. J Apic Res 53:269–278
Reich DE et al (2002) Human genome sequence variation and the influence of gene history, mutation and recombination. Nat Genet 32:135
Ritz KR, Noor MA, Singh ND (2017) Variation in recombination rate: adaptive or not? Trends Genet 33:364–374
Robertson HM, Wanner KW (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res 16:1395–1403
Ross C, DeFelice D, Hunt G, Ihle K, Rueppell O (2015a) A comparison of multiple genome-wide recombination maps in Apis mellifera. Collaborative mathematics and statistics research. Springer, Berlin, pp 91–98
Ross CR, DeFelice DS, Hunt GJ, Ihle KE, Amdam GV, Rueppell O (2015b) Genomic correlates of recombination rate and its variability across eight recombination maps in the western honey bee (Apis mellifera L.). BMC Genom 16:107
Ross L, Blackmon H, Lorite P, Gokhman V, Hardy N (2015c) Recombination, chromosome number and eusociality in the Hymenoptera. J Evol Biol 28:105–116
Rueppell O, Meier S, Deutsch R (2012) Multiple mating but not recombination causes quantitative increase in offspring genetic diversity for varying genetic architectures. PLoS One 7:e47220
Rueppell O et al (2016) A new metazoan recombination rate record and consistently high recombination rates in the honey bee genus Apis accompanied by frequent inversions but not translocations. Genome Biol Evol 8:3653–3660
Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin
Schneider SS, DeGrandi-Hoffman G, Smith DR (2004) The African honey bee: factors contributing to a successful biological invasion. Annu Rev Entomol 49:351–376
Shi YY, Sun LX, Huang ZY, Wu XB, Zhu YQ, Zheng HJ, Zeng ZJ (2013) A SNP based high-density linkage map of Apis cerana reveals a high recombination rate similar to Apis mellifera. PLoS One 8:e76459
Sirviö A, Gadau J, Rueppell O, Lamatsch D, Boomsma JJ, Pamilo P, Page RE (2006) High recombination frequency creates genotypic diversity in colonies of the leaf-cutting ant Acromyrmex echinatior. J Evol Biol 19:1475–1485
Sirviö A, Johnston JS, Wenseleers T, Pamilo P (2011) A high recombination rate in eusocial Hymenoptera: evidence from the common wasp Vespula vulgaris. BMC Genet 12:95
Smukowski CS, Noor MAF (2011) Recombination rate variation in closely related species. Heredity 107:496–508
Solignac M, Mougel F, Vautrin D, Monnerot M, Cornuet JM (2007) A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol 8:R66
Southwick EE, Heldmaier G (1987) Temperature control in honey bee colonies. Bioscience 37:395–399
Stapley J, Feulner PG, Johnston SE, Santure AW, Smadja CM (2017) Variation in recombination frequency and distribution across eukaryotes: patterns and processes. Philos Trans R Soc B 372:20160455
Stevison LS, Sefick S, Rushton C, Graze RM (2017) Recombination rate plasticity: revealing mechanisms by design. Philos Trans R Soc B 372:20160459
Tarpy DR, Seeley TD (2006) Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93:195–199
Tundo GR et al (2017) Multiple functions of insulin-degrading enzyme: a metabolic crosslight? Crit Rev Biochem Mol Biol 52:554–582
Ubeda F, Wilkins JF (2011) The Red Queen theory of recombination hotspots. J Evol Biol 24:541–553
Van Oers K et al (2014) Replicated high-density genetic maps of two great tit populations reveal fine-scale genomic departures from sex-equal recombination rates. Heredity 112:307
Wallberg A et al (2014) A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera. Nat Genet 46:1081–1090
Wallberg A, Glémin S, Webster MT (2015) Extreme recombination frequencies shape genome variation and evolution in the Honeybee, Apis mellifera. PLoS Genet 11:e1005189
Wallberg A et al (2019) A hybrid de novo genome assembly of the honeybee, Apis mellifera, with chromosome-length scaffolds. BMC Genom 20:275
Wilfert L, Gadau J, Schmid-Hempel P (2007) Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity 98:189–197
Williams CG, Goodman MM, Stuber CW (1995) Comparative recombination distances among Zea mays L. inbreds, wide crosses and interspecific hybrids. Genetics 141:1573–1581
Acknowledgements
We would like to thank all instructors and fellow students of the Math-Bio REU-site at UNCG for their support and collegial working atmosphere. We appreciate the opportunity to sample “Russian” colonies from Steven Coy (then President of the Russian Honey Bee Breeders) in Perkinston, Mississippi. We would like to thank Sharon Furiness and the Genomics Core Lab at TAMU Corpus Christi for performing the ddRAD library preparation, SE sequencing, and SNP extraction. Esmaeil Amiri assisted in the data management. We would also like to thank three anonymous reviewers whose comments on a previous version of this manuscript helped us to improve the presentation of our study. Research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institutes of Health under award number R15GM102753. Further financial support was provided by the US National Science Foundation (DMS #1359187) and UNCG.
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DeLory, T., Funderburk, K., Miller, K. et al. Local variation in recombination rates of the honey bee (Apis mellifera) genome among samples from six disparate populations. Insect. Soc. 67, 127–138 (2020). https://doi.org/10.1007/s00040-019-00736-6
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DOI: https://doi.org/10.1007/s00040-019-00736-6