Fitness
Fine-scale contemporary recombination variation and its fitness consequences in adaptively diverging stickleback fish – Nature Ecology & Evolution
Hassold, T. & Hunt, P. To ERR (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2, 280–291 (2001).
Inoue, K. & Lupski, J. R. Molecular mechanisms for genomic disorders. Ann. Rev. Genomics Hum. Genet. 3, 199–242 (2002).
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).
Paigen, K. et al. The recombinational anatomy of a mouse chromosome. PLoS Genet. 4, e1000119 (2008).
Kong, A. et al. Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467, 1099–1103 (2010).
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).
Lenormand, T. & Dutheil, J. Recombination difference between sexes: a role for haploid selection. PLoS Biol. 3, e63 (2005).
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).
Sardell, J. M. et al. Sex differences in recombination in sticklebacks. G3 8, 1971–G83 (2018).
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).
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).
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).
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).
Kaur, T. & Rockman, M. V. Crossover heterogeneity in the absence of hotspots in Caenorhabditis elegans. Genetics. 196, 137–148 (2014).
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).
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).
Choi, K. & Henderson, I. R. Meiotic recombination hotspots—a comparative view. Plant J. 83, 52–61 (2015).
Giraut, L. et al. Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet. 7, e1002354 (2011).
Pan, J. et al. A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144, 719–731 (2011).
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).
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).
Kong, A. et al. Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319, 1398–1401 (2008).
Reynolds, A. et al. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat. Genet. 45, 269–278 (2013).
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).
Baudat, F. et al. PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327, 836–840 (2010).
Myers, S. et al. Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327, 876–879 (2010).
Parvanov, E. D., Petkov, P. M. & Paigen, K. Prdm9 controls activation of mammalian recombination hotspots. Science 327, 835 (2010).
Charlesworth, D. & Charlesworth, B. Selection on recombination in clines. Genetics. 91, 581–589 (1979).
Rodell, C. F., Schipper, M. R. & Keenan, D. K. Modes of selection and recombination response in Drosophila melanogaster. J. Hered. 95, 70–75 (2004).
Coop, G. & Przeworski, M. An evolutionary view of human recombination. Nat. Rev. Genet. 8, 23–34 (2007).
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).
Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012).
Supple, M. A. et al. Genomic architecture of adaptive color pattern divergence and convergence in Heliconius butterflies. Genome Res. 23, 1248–1257 (2013).
Marques, D. A. et al. Genomics of rapid incipient speciation in sympatric threespine stickleback. PLoS Genet. 12, e1005887 (2016).
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).
Colosimo, P. F. et al. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307, 1928–1933 (2005).
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).
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).
Kirkpatrick, M. & Barton, N. Chromosome inversions, local adaptation and speciation. Genetics. 173, 419–434 (2006).
Charlesworth, B. & Barton, N. H. The spread of an inversion with migration and selection. Genetics. 208, 377–382 (2018).
Roesti, M., Moser, D. & Berner, D. Recombination in the threespine stickleback genome—patterns and consequences. Mol. Ecol. 22, 3014–3027 (2013).
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).
Baker, Z. et al. Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates. eLife. 6, e24133 (2017).
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).
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).
Brandvain, Y. & Coop, G. Scrambling eggs: meiotic drive and the evolution of female recombination rates. Genetics 190, 709–723 (2012).
Ma, L. et al. Cattle sex-specific recombination and genetic control from a large pedigree analysis. PLoS Genet. 11, e1005387 (2015).
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).
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).
Paigen, K. & Petkov, P. Mammalian recombination hot spots: properties, control and evolution. Nat. Rev. Genet. 11, 221–233 (2010).
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).
Guillon, H., Grey, C., Liskay, M. R. & de Massy, B. Crossover and noncrossover pathways in mouse meiosis. Mol. Cell 20, 563–573 (2005).
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).
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).
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).
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).
Borgogno, M. V. et al. Tolerance of DNA Mismatches in Dmc1 recombinase-mediated DNA strand exchange. J. Biol. Chem. 291, 4928–4938 (2016).
Hinch, A. G. et al. Factors influencing meiotic recombination revealed by whole-genome sequencing of single sperm. Science 363, 6433 (2019).
Schluter, D. et al. Fitness maps to a large-effect locus in introduced stickleback populations. Proc. Natl Acad. Sci. USA 118, e1914889118 (2021).
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).
Peichel, C. L. & Marques, D. A. The genetic and molecular architecture of phenotypic diversity in sticklebacks. Phil. Trans. R. Soc. B 372, 20150486 (2017).
Verta, J. P. & Jones, F. C. Predominance of cis-regulatory changes in parallel expression divergence of sticklebacks. eLife 8, e43785 (2019).
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).
McVean, G. A. et al. The fine-scale structure of recombination rate variation in the human genome. Science 304, 581–584 (2004).
Chan, A. H., Jenkins, P. A. & Song, Y. S. Genome-wide fine-scale recombination rate variation in Drosophila melanogaster. PLoS Genet. 8, e1003090 (2012).
Singhal, S. et al. Stable recombination hotspots in birds. Science 350, 928–932 (2015).
Pazhayam, N. M., Turcotte, C. A. & Sekelsky, J. Meiotic crossover patterning. Front. Cell Dev. Biol. 9, 681123 (2021).
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).
Auton, A. et al. Genetic recombination is targeted towards gene promoter regions in dogs. PLoS Genet. 9, e1003984 (2013).
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).
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).
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).
DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491 (2011).
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).
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).
Delaneau, O., Marchini, J. & Zagury, J. F. A linear complexity phasing method for thousands of genomes. Nat. Methods 9, 179–181 (2011).
O’Connell, J. et al. A general approach for haplotype phasing across the full spectrum of relatedness. PLoS Genet. 10, e1004234 (2014).
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).
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).
Smagulova, F. et al. Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472, 375–378 (2011).
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
Zhang, Y. et al. Model-based analysis of ChIP-seq (MACS). Genome Biol. 9, R137 (2008).
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).
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).
Greenwood, A. K. et al. Genetic mapping of natural variation in schooling tendency in the threespine stickleback. G3 5, 761–769 (2015).
Cech, J. N. & Peichel, C. L. Identification of the centromeric repeat in the threespine stickleback fish (Gasterosteus aculeatus). Chromosome Res. 23, 767–779 (2015).
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).