Friday, November 22, 2024

Fine-scale contemporary recombination variation and its fitness consequences in adaptively diverging stickleback fish – Nature Ecology & Evolution

Must read

  • Hassold, T. & Hunt, P. To ERR (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2, 280–291 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Inoue, K. & Lupski, J. R. Molecular mechanisms for genomic disorders. Ann. Rev. Genomics Hum. Genet. 3, 199–242 (2002).

    Article 
    CAS 

    Google Scholar
     

  • Wang, S., Zickler, D., Kleckner, N. & Zhang, L. Meiotic crossover patterns: obligatory crossover, interference and homeostasis in a single process. Cell Cycle 14, 305–314 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Paigen, K. et al. The recombinational anatomy of a mouse chromosome. PLoS Genet. 4, e1000119 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kong, A. et al. Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467, 1099–1103 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Broman, K. W., Murray, J. C., Sheffield, V. C., White, R. L. & Weber, J. L. Comprehensive human genetic maps: individual and sex-specific variation in recombination. Am. J. Hum. Genet. 63, 861–869 (1998).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

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

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shifman, S. B. J., Copley, R. R., Taylor, M. S. & Williams, R. W. A high-resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biol. 4, e395 (2006).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sardell, J. M. et al. Sex differences in recombination in sticklebacks. G3 8, 1971–G83 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Coop, G., Wen, X., Ober, C., Pritchard, J. K. & Przeworski, M. High-resolution mapping of crossovers reveals extensive variation in fine-scale recombination patterns among humans. Science 319, 1395–1398 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dumont, B. L., White, M. A., Steffy, B., Wiltshire, T. & Payseur, B. A. Extensive recombination rate variation in the house mouse species complex inferred from genetic linkage maps. Genome Res. 21, 114–125 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stapley, J., Feulner, P. G. D., Johnston, S. E., Santure, A. W. & Smadja, C. M. Variation in recombination frequency and distribution across eukaryotes: patterns and processes. Phil. Trans. R. Soc. B 372, 20160455 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Manzano-Winkler, B., McGaugh, S. E. & Noor, M. A. How hot are drosophila hotspots? examining recombination rate variation and associations with nucleotide diversity, divergence, and maternal age in Drosophila pseudoobscura. PLoS ONE 8, e71582 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kaur, T. & Rockman, M. V. Crossover heterogeneity in the absence of hotspots in Caenorhabditis elegans. Genetics. 196, 137–148 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Myers, S., Bottolo, L., Freeman, C., McVean, G. & Donnelly, P. A fine-scale map of recombination rates and hotspots across the human genome. Science 310, 321–324 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mancera, E., Bourgon, R., Brozzi, A., Huber, W. & Steinmetz, L. M. High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454, 479–485 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Choi, K. & Henderson, I. R. Meiotic recombination hotspots—a comparative view. Plant J. 83, 52–61 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Giraut, L. et al. Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet. 7, e1002354 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pan, J. et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144, 719–731 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tischfield, S. E. & Keeney, S. Scale matters: the spatial correlation of yeast meiotic DNA breaks with histone H3 trimethylation is driven largely by independent colocalization at promoters. Cell Cycle 11, 1496–1503 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shilo, S., Melamed-Bessudo, C., Dorone, Y., Barkai, N. & Levy, A. A. DNA crossover motifs associated with epigenetic modifications delineate open chromatin regions in Arabidopsis. Plant Cell 27, 2427–2436 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kong, A. et al. Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319, 1398–1401 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Reynolds, A. et al. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat. Genet. 45, 269–278 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Johnston, S. E., Berenos, C., Slate, J. & Pemberton, J. M. Conserved genetic architecture underlying individual recombination rate variation in a wild population of soay sheep (Ovis aries). Genetics. 203, 583–598 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Baudat, F. et al. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327, 836–840 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Myers, S. et al. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327, 876–879 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Parvanov, E. D., Petkov, P. M. & Paigen, K. Prdm9 controls activation of mammalian recombination hotspots. Science 327, 835 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Charlesworth, D. & Charlesworth, B. Selection on recombination in clines. Genetics. 91, 581–589 (1979).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rodell, C. F., Schipper, M. R. & Keenan, D. K. Modes of selection and recombination response in Drosophila melanogaster. J. Hered. 95, 70–75 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

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

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pritchard, J. K., Pickrell, J. K. & Coop, G. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr. Biol. 20, R208–R215 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Supple, M. A. et al. Genomic architecture of adaptive color pattern divergence and convergence in Heliconius butterflies. Genome Res. 23, 1248–1257 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Marques, D. A. et al. Genomics of rapid incipient speciation in sympatric threespine stickleback. PLoS Genet. 12, e1005887 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Roda, F., Walter, G. M., Nipper, R. & Ortiz-Barrientos, D. Genomic clustering of adaptive loci during parallel evolution of an Australian wildflower. Mol. Ecol. 26, 3687–3699 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Colosimo, P. F. et al. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307, 1928–1933 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bell, M. A. & Foster, S. A. The Evolutionary Biology of the Threespine Stickleback 571 (Oxford Univ. Press, 1994).

  • Terekhanova, N. V. et al. Fast evolution from precast bricks: genomics of young freshwater populations of threespine stickleback Gasterosteus aculeatus. PLoS Genet. 10, e1004696 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kirch, M., Romundset, A., Gilbert, M. T. P., Jones, F. C. & Foote, A. D. Ancient and modern stickleback genomes reveal the demographic constraints on adaptation. Curr. Biol. 31, 2027–2036 e8 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kirkpatrick, M. & Barton, N. Chromosome inversions, local adaptation and speciation. Genetics. 173, 419–434 (2006).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Charlesworth, B. & Barton, N. H. The spread of an inversion with migration and selection. Genetics. 208, 377–382 (2018).

    Article 
    PubMed 

    Google Scholar
     

  • Roesti, M., Moser, D. & Berner, D. Recombination in the threespine stickleback genome—patterns and consequences. Mol. Ecol. 22, 3014–3027 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Samuk, K., Delmore, K. E., Miller, S. E., Rennison, D. J. & Schluter, D. Gene flow and selection interact to promote adaptive divergence in regions of low recombination. Mol. Ecol. 26, 4378–4390 (2017).

    Article 
    PubMed 

    Google Scholar
     

  • Baker, Z. et al. Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates. eLife. 6, e24133 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shanfelter, A. F., Archambeault, S. L. & White, M. A. Divergent fine-scale recombination landscapes between a freshwater and marine population of threespine stickleback fish. Genome Biol. Evol. 11, 1573–1585 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Rastas, P., Calboli, F. C., Guo, B., Shikano, T. & Merila, J. Construction of ultradense linkage maps with Lep-MAP2: stickleback F2 recombinant crosses as an example. Genome Biol. Evol. 8, 78–93 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brandvain, Y. & Coop, G. Scrambling eggs: meiotic drive and the evolution of female recombination rates. Genetics 190, 709–723 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ma, L. et al. Cattle sex-specific recombination and genetic control from a large pedigree analysis. PLoS Genet. 11, e1005387 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Johnston, S. E., Huisman, J., Ellis, P. A. & Pemberton, J. M. A high-density linkage map reveals sexual dimorphism in recombination landscapes in red deer (Cervus elaphus). G3 7, 2859–2870 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Samuk, K., Manzano-Winkler, B., Ritz, K. R. & Noor, M. A. F. Natural selection shapes variation in genome-wide recombination rate in Drosophila pseudoobscura. Curr. Biol. 30, 1517–28 e6 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Paigen, K. & Petkov, P. Mammalian recombination hot spots: properties, control and evolution. Nat. Rev. Genet. 11, 221–233 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Szostak, J. W., Orr-Weaver, T. L., Rothstein, R. J. & Stahl, F. W. The double-strand-break repair model for recombination. Cell. 33, 25–35 (1983).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Guillon, H., Grey, C., Liskay, M. R. & de Massy, B. Crossover and noncrossover pathways in mouse meiosis. Mol. Cell 20, 563–573 (2005).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Székvölgyi, L. Ohta, K. & Nicolas, A. Initiation of meiotic homologous recombination: flexibility, impact of histone modifications, and chromatin remodeling. Cold Spring Harb. Perspect. Biol. https://doi.org/10.1101/cshperspect.a016527 (2015).

  • Khil, P. P., Smagulova, F., Brick, K. M., Camerini-Otero, R. D. & Petukhova, G. V. Sensitive mapping of recombination hotspots using sequencing-based detection of ssDNA. Genome Res. 22, 957–965 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nath, S., Welch, L. A., Flanagan, M. K. & White, M. A. Meiotic pairing and double-strand break formation along the heteromorphic threespine stickleback sex chromosomes. Chromosome Res. 30, 429–442 (2022).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schwarzacher, T. Meiosis, recombination and chromosomes: a review of gene isolation and fluorescent in situ hybridization data in plants. J. Exp. Bot. 54, 11–23 (2003).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dreau, A., Venu, V., Avdievich, E., Gaspar, L. & Jones, F. C. Genome-wide recombination map construction from single individuals using linked-read sequencing. Nat. Commun. 10, 4309 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Borgogno, M. V. et al. Tolerance of DNA Mismatches in Dmc1 recombinase-mediated DNA strand exchange. J. Biol. Chem. 291, 4928–4938 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hinch, A. G. et al. Factors influencing meiotic recombination revealed by whole-genome sequencing of single sperm. Science 363, 6433 (2019).

    Article 

    Google Scholar
     

  • Schluter, D. et al. Fitness maps to a large-effect locus in introduced stickleback populations. Proc. Natl Acad. Sci. USA 118, e1914889118 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Roberts Kingman, G. A. et al. Longer or shorter spines: reciprocal trait evolution in stickleback via triallelic regulatory changes in Stanniocalcin2a. Proc. Natl Acad. Sci. USA 118, e2100694118 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Peichel, C. L. & Marques, D. A. The genetic and molecular architecture of phenotypic diversity in sticklebacks. Phil. Trans. R. Soc. B 372, 20150486 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Verta, J. P. & Jones, F. C. Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks. eLife 8, e43785 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jones, F. C., Brown, C., Pemberton, J. M. & Braithwaite, V. A. Reproductive isolation in a threespine stickleback hybrid zone. J. Evol. Biol. 19, 1531–1544 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • McVean, G. A. et al. The fine-scale structure of recombination rate variation in the human genome. Science 304, 581–584 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chan, A. H., Jenkins, P. A. & Song, Y. S. Genome-wide fine-scale recombination rate variation in Drosophila melanogaster. PLoS Genet. 8, e1003090 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Singhal, S. et al. Stable recombination hotspots in birds. Science 350, 928–932 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pazhayam, N. M., Turcotte, C. A. & Sekelsky, J. Meiotic crossover patterning. Front. Cell Dev. Biol. 9, 681123 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bass, H. W. et al. Evidence for the coincident initiation of homolog pairing and synapsis during the telomere-clustering (bouquet) stage of meiotic prophase. J. Cell. Sci. 113, 1033–1042 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Auton, A. et al. Genetic recombination is targeted towards gene promoter regions in dogs. PLoS Genet. 9, e1003984 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brick, K., Smagulova, F., Khil, P., Camerini-Otero, R. D. & Petukhova, G. V. Genetic recombination is directed away from functional genomic elements in mice. Nature 485, 642–645 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kieleczawa, J. DNA Sequencing II: Optimizing Preparation and Cleanup (Jones and Bartlett, 2006).

  • Bronner, I. F., Quail, M. A., Turner, D. J. & Swerdlow, H. Improved protocols for Illumina sequencing. Curr. Protoc. Hum. Genet. 80, 18 (2014).


    Google Scholar
     

  • Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Scrucca, L., Fop, M., Murphy, T. B. & Raftery, A. E. mclust 5: clustering, classification and density estimation using Gaussian finite mixture models. R J. 8, 289–317 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Glazer, A. M., Killingbeck, E. E., Mitros, T., Rokhsar, D. S. & Miller, C. T. Genome assembly improvement and mapping convergently evolved skeletal traits in sticklebacks with genotyping-by-sequencing. G3 5, 1463–1472 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Delaneau, O., Marchini, J. & Zagury, J. F. A linear complexity phasing method for thousands of genomes. Nat. Methods 9, 179–181 (2011).

    Article 
    PubMed 

    Google Scholar
     

  • O’Connell, J. et al. A general approach for haplotype phasing across the full spectrum of relatedness. PLoS Genet. 10, e1004234 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing https://www.R-project.org/ (2021).

  • Osoegawa, K., Mack, S. J., Prestegaard, M. & Fernandez-Vina, M. A. Tools for building, analyzing and evaluating HLA haplotypes from families. Hum. Immunol. 80, 633–643 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Borg, B. Seasonal effects of photoperiod and temperature on spermatogenesis and male secondary sexual characters in the three-spined stickleback, Gasterosteus aculeatus L. Can. J. Zool. 60, 3377–3386 (1982).

    Article 

    Google Scholar
     

  • Smagulova, F. et al. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472, 375–378 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, Y. et al. Model-based analysis of ChIP-seq (MACS). Genome Biol. 9, R137 (2008).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Buenrostro, J. D., Wu, B., Chang, H. Y. & Greenleaf, W. J. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr. Protoc. Mol. Biol. 109, 2191–2199 (2015).

    Article 

    Google Scholar
     

  • Venu, V. et al. Fine-scale contemporary recombination variation and its fitness consequences in adaptively diverging stickleback fish. GitHub https://github.com/felicitycjones/Venu_SticklebackRecombination/tree/main (2024).

  • Rogers, S. M. et al. Genetic signature of adaptive peak shift in threespine stickleback. Evolution 66, 2439–2450 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Greenwood, A. K. et al. Genetic mapping of natural variation in schooling tendency in the threespine stickleback. G3 5, 761–769 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cech, J. N. & Peichel, C. L. Identification of the centromeric repeat in the threespine stickleback fish (Gasterosteus aculeatus). Chromosome Res. 23, 767–779 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Singh, N. D., Stone, E. A., Aquadro, C. F. & Clark, A. G. Fine-scale heterogeneity in crossover rate in the garnet-scalloped region of the Drosophila melanogaster X chromosome. Genetics 194, 375–387 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Latest article