in

Intercontinental genomic parallelism in multiple three-spined stickleback adaptive radiations

  • 1.

    Schluter, D. The Ecology of Adaptive Radiations (Oxford Univ. Press, 2000).

  • 2.

    Gavrilets, S. & Losos, J. B. Adaptive radiation: contrasting theory with data. Science 323, 732–737 (2009).

    CAS  PubMed  Google Scholar 

  • 3.

    Arnold, S. J., Bürger, R., Hohenlohe, P. A., Ajie, B. C. & Jones, A. G. Understanding the evolution and stability of the G-matrix. Evolution 62, 2451–2461 (2008).

    PubMed  PubMed Central  Google Scholar 

  • 4.

    Losos, J. B. Adaptive radiation, ecological opportunity, and evolutionary determinism: American Society of Naturalists E. O. Wilson award address. Am. Nat. 175, 623–639 (2010).

    PubMed  Google Scholar 

  • 5.

    Elmer, K. R. et al. Parallel evolution of Nicaraguan crater lake cichlid fishes via non-parallel routes. Nat. Commun. 5, 5168 (2014).

    CAS  PubMed  Google Scholar 

  • 6.

    Mahler, D. L., Ingram, T., Revell, L. J. & Losos, J. B. Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science 341, 292–295 (2013).

    CAS  PubMed  Google Scholar 

  • 7.

    Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015).

    CAS  PubMed  Google Scholar 

  • 8.

    Gould, S. J. Wonderful Life: The Burgess Shale and the Nature of History (W. W. Norton, 1989).

  • 9.

    Schluter, D. Adaptive radiation along genetic lines of least resistance. Evolution 50, 1766–1774 (1996).

    PubMed  Google Scholar 

  • 10.

    Roff, D. The evolution of the G matrix: selection or drift? Heredity 84, 135–142 (2000).

    PubMed  Google Scholar 

  • 11.

    Arendt, J. & Reznick, D. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23, 26–32 (2008).

    PubMed  Google Scholar 

  • 12.

    Stuart, Y. E. Divergent uses of ‘parallel evolution’ during the history of the American naturalist. Am. Nat. 193, 11–19 (2019).

    PubMed  Google Scholar 

  • 13.

    Oke, K. B., Rolshausen, G., LeBlond, C. & Hendry, A. P. How parallel is parallel evolution? A comparative analysis in fishes. Am. Nat. 190, 1–16 (2017).

    PubMed  Google Scholar 

  • 14.

    McGee, M. D., Neches, R. Y. & Seehausen, O. Evaluating genomic divergence and parallelism in replicate ecomorphs from young and old cichlid adaptive radiations. Mol. Ecol. 25, 260–268 (2016).

    CAS  PubMed  Google Scholar 

  • 15.

    Soria-Carrasco, V. et al. Stick insect genomes reveal natural selection’s role in parallel speciation. Science 344, 738–742 (2014).

    CAS  PubMed  Google Scholar 

  • 16.

    MacColl, A. D. C. The ecological causes of evolution. Trends Ecol. Evol. 26, 514–522 (2011).

    PubMed  Google Scholar 

  • 17.

    Elmer, K. R. & Meyer, A. Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol. Evol. 26, 298–306 (2011).

    PubMed  Google Scholar 

  • 18.

    Conte, G. L., Arnegard, M. E., Peichel, C. L. & Schluter, D. The probability of genetic parallelism and convergence in natural populations. Proc. R. Soc. B 279, 5039–5047 (2012).

    PubMed  Google Scholar 

  • 19.

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 20.

    Stuart, Y. E. et al. Contrasting effects of environment and genetics generate a continuum of parallel evolution. Nat. Ecol. Evol. 1, 0158 (2017).

    Google Scholar 

  • 21.

    Jacobs, A. et al. Parallelism in eco-morphology and gene expression despite variable evolutionary and genomic backgrounds in a Holarctic fish. PLoS Genet. 16, 1008658 (2020).

    Google Scholar 

  • 22.

    Muschick, M., Indermaur, A. & Salzburger, W. Convergent evolution within an adaptive radiation of cichlid fishes. Curr. Biol. 22, 2362–2368 (2012).

    CAS  Google Scholar 

  • 23.

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

  • 24.

    Taylor, E. B. & McPhail, J. D. Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc. R. Soc. Lond. B 267, 2375–2384 (2000).

    CAS  Google Scholar 

  • 25.

    Kaeuffer, R., Peichel, C. L., Bolnick, D. I. & Hendry, A. P. Parallel and nonparallel aspects of ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback. Evolution 66, 402–418 (2012).

    PubMed  Google Scholar 

  • 26.

    Ravinet, M., Prodöhl, P. A. & Harrod, C. Parallel and nonparallel ecological, morphological and genetic divergence in lake-stream stickleback from a single catchment. J. Evol. Biol. 26, 186–204 (2013).

    CAS  PubMed  Google Scholar 

  • 27.

    Magalhaes, I. S., D’Agostino, D., Hohenlohe, P. A. & MacColl, A. D. C. The ecology of an adaptive radiation of three-spined stickleback from North Uist, Scotland. Mol. Ecol. 25, 4319–4336 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 28.

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

    CAS  PubMed  Google Scholar 

  • 29.

    Jones, F. C. et al. A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr. Biol. 22, 83–90 (2012).

    CAS  PubMed  Google Scholar 

  • 30.

    Raeymaekers, J. A. M. et al. Adaptive and non-adaptive divergence in a common landscape. Nat. Commun. 8, 267 (2017).

    PubMed  PubMed Central  Google Scholar 

  • 31.

    Rennison, D. J., Stuart, Y. E., Bolnick, D. I. & Peichel, C. L. Ecological factors and morphological traits are associated with repeated genomic differentiation between lake and stream stickleback. Phil. Trans. R. Soc. B 374, 20180241 (2019).

    CAS  PubMed  Google Scholar 

  • 32.

    MacColl, A. D. C. & Aucott, B. Inappropriate analysis does not reveal the ecological causes of evolution of stickleback armour: a critique of Spence et al. 2013. Ecol. Evol. 4, 3509–3513 (2014).

    PubMed  PubMed Central  Google Scholar 

  • 33.

    Spoljaric, M. A. & Reimchen, T. E. 10,000 years later: evolution of body shape in Haida Gwaii three-spined stickleback. J. Fish Biol. 70, 1484–1503 (2007).

    Google Scholar 

  • 34.

    De Schamphelaere, K. A. C. et al. Reproductive toxicity of dietary zinc to Daphnia magna. Aquat. Toxicol. 70, 233–244 (2004).

    PubMed  Google Scholar 

  • 35.

    Martins, C., Jesus, F. T. & Nogueira, A. J. A. The effects of copper and zinc on survival, growth and reproduction of the cladoceran Daphnia longispina: introducing new data in an ‘old’ issue. Ecotoxicology 26, 1157–1169 (2017).

    CAS  PubMed  Google Scholar 

  • 36.

    Miller, C. T. et al. Modular skeletal evolution in sticklebacks is controlled by additive and clustered quantitative trait loci. Genetics 197, 405–420 (2014).

    PubMed  PubMed Central  Google Scholar 

  • 37.

    Chan, Y. F. et al. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327, 302–305 (2010).

    CAS  PubMed  Google Scholar 

  • 38.

    Thompson, K. A., Osmond, M. M. & Schluter, D. Parallel genetic evolution and speciation from standing variation. Evol. Lett. 3, 129–141 (2019).

    PubMed  PubMed Central  Google Scholar 

  • 39.

    Nelson, T. C. & Cresko, W. A. Ancient genomic variation underlies repeated ecological adaptation in young stickleback populations. Evol. Lett. 2, 9–21 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 40.

    Paccard, A. et al. Repeatability of adaptive radiation depends on spatial scale: regional versus global replicates of stickleback in lake versus stream habitats. J. Hered. 111, 43–56 (2019).

    Google Scholar 

  • 41.

    Baldo, L., Riera, J. L., Salzburger, W. & Barluenga, M. Phylogeography and ecological niche shape the cichlid fish gut microbiota in Central American and African lakes. Front. Microbiol. 10, 2372 (2019).

    PubMed  PubMed Central  Google Scholar 

  • 42.

    Fang, B., Kemppainen, P., Momigliano, P. & Merilä, J. On the causes of geographically heterogeneous parallel evolution in sticklebacks. Nat. Ecol. Evol. 4, 1105–1115 (2020).

    PubMed  Google Scholar 

  • 43.

    Mäkinen, H. S. & Merilä, J. Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe—evidence for multiple glacial refugia. Mol. Phylogenet. Evol. 46, 167–182 (2008).

    PubMed  Google Scholar 

  • 44.

    Liu, S., Hansen, M. M. & Jacobsen, M. W. Region-wide and ecotype-specific differences in demographic histories of threespine stickleback populations, estimated from whole genome sequences. Mol. Ecol. 25, 5187–5202 (2016).

    CAS  PubMed  Google Scholar 

  • 45.

    Fang, B., Merilä, J., Ribeiro, F., Alexandre, C. M. & Momigliano, P. Worldwide phylogeny of three-spined sticklebacks. Mol. Phylogenet. Evol. 127, 613–625 (2018).

    PubMed  Google Scholar 

  • 46.

    Garduno-Paz, M. V., Couderc, S. & Adams, C. E. Habitat complexity modulates phenotype expression through developmental plasticity in the threespine stickleback. Biol. J. Linn. Soc. 100, 407–413 (2010).

    Google Scholar 

  • 47.

    Coop, G., Witonsky, D., Di Rienzo, A. & Pritchard, J. K. Using environmental correlations to identify loci underlying local adaptation. Genetics 185, 1411–1423 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 48.

    Hohenlohe, P. A. et al. Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6, e1000862 (2010).

    PubMed  PubMed Central  Google Scholar 

  • 49.

    Guo, B., DeFaveri, J., Sotelo, G., Nair, A. & Merilä, J. Population genomic evidence for adaptive differentiation in Baltic Sea three-spined sticklebacks. BMC Biol. 13, 19 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 50.

    Glazer, A. M., Cleves, P. A., Erickson, P. A., Lam, A. Y. & Miller, C. T. Parallel developmental genetic features underlie stickleback gill raker evolution. EvoDevo 5, 19 (2014).

    PubMed  PubMed Central  Google Scholar 

  • 51.

    Day, T., Pritchard, J. & Schluter, D. A comparison of two sticklebacks. Evolution 48, 1723–1734 (1994).

    PubMed  Google Scholar 

  • 52.

    Franchini, P. et al. Genomic architecture of ecologically divergent body shape in a pair of sympatric crater lake cichlid fishes. Mol. Ecol. 23, 1828–1845 (2014).

    PubMed  Google Scholar 

  • 53.

    McCairns, R. J. S. & Bernatchez, L. Plasticity and heritability of morphological variation within and between parapatric stickleback demes. J. Evol. Biol. 25, 1097–1112 (2012).

    CAS  PubMed  Google Scholar 

  • 54.

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

    PubMed  Google Scholar 

  • 55.

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

    PubMed  PubMed Central  Google Scholar 

  • 56.

    Burke, M. K., Liti, G. & Long, A. D. Standing genetic variation drives repeatable experimental evolution in outcrossing populations of Saccharomyces cerevisiae. Mol. Biol. Evol. 31, 3228–3239 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 57.

    Kang, L., Aggarwal, D. D., Rashkovetsky, E., Korol, A. B. & Michalak, P. Rapid genomic changes in Drosophila melanogaster adapting to desiccation stress in an experimental evolution system. BMC Genom. 17, 233 (2016).

    Google Scholar 

  • 58.

    Gompert, Z. & Messina, F. J. Genomic evidence that resource‐based trade‐offs limit host‐range expansion in a seed beetle. Evolution 70, 1249–1264 (2016).

    CAS  PubMed  Google Scholar 

  • 59.

    Berner, D., Moser, D., Roesti, M., Buescher, H. & Salzburger, W. Genetic architecture of skeletal evolution in European lake and stream stickleback. Evolution 68, 1792–1805 (2014).

    CAS  PubMed  Google Scholar 

  • 60.

    Pease, J. B., Haak, D. C., Hahn, M. W. & Moyle, L. C. Phylogenomics reveals three sources of adaptive variation during a rapid radiation. PLoS Biol. 14, e1002379 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 61.

    Lowry, D. B. et al. Breaking RAD: an evaluation of the utility of restriction site-associated DNA sequencing for genome scans of adaptation. Mol. Ecol. Resour. 17, 142–152 (2017).

    CAS  Google Scholar 

  • 62.

    McKinney, G. J., Larson, W. A., Seeb, L. W. & Seeb, J. E. RADseq provides unprecedented insights into molecular ecology and evolutionary genetics: comment on Breaking RAD by Lowry et al. (2016). Mol. Ecol. Resour. 17, 356–361 (2017).

    CAS  PubMed  Google Scholar 

  • 63.

    Roesti, M., Kueng, B., Moser, D. & Berner, D. The genomics of ecological vicariance in threespine stickleback fish. Nat. Commun. 6, 8767 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 64.

    Catchen, J. M. et al. Unbroken: RADseq remains a powerful tool for understanding the genetics of adaptation in natural populations. Mol. Ecol. Resour. 17, 362–365 (2017).

    CAS  PubMed  Google Scholar 

  • 65.

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

    CAS  PubMed  Google Scholar 

  • 66.

    Samuk, K. et al. Gene flow and selection interact to promote adaptive divergence in regions of low recombination. Mol. Ecol. 26, 4378–4390 (2017).

    PubMed  Google Scholar 

  • 67.

    Meier, J. I., Marques, D. A., Wagner, C. E., Excoffier, L. & Seehausen, O. Genomics of parallel ecological speciation in Lake Victoria cichlids. Mol. Biol. Evol. 35, 1489–1506 (2018).

    CAS  PubMed  Google Scholar 

  • 68.

    Cruickshank, T. E. & Hahn, M. W. Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol. Ecol. 23, 3133–3157 (2014).

    PubMed  Google Scholar 

  • 69.

    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).

    PubMed  PubMed Central  Google Scholar 

  • 70.

    Westram, A. M. et al. Clines on the seashore: the genomic architecture underlying rapid divergence in the face of gene flow. Evol. Lett. 2, 297–309 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 71.

    Shimada, Y., Shikano, T. & Merilä, J. A high incidence of selection on physiologically important genes in the three-spined stickleback, Gasterosteus aculeatus. Mol. Biol. Evol. 28, 181–193 (2011).

    CAS  PubMed  Google Scholar 

  • 72.

    Xie, K. T. et al. DNA fragility in the parallel evolution of pelvic reduction in stickleback fish. Science 363, 81–84 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 73.

    Henning, F. & Meyer, A. The evolutionary genomics of cichlid fishes: explosive speciation and adaptation in the postgenomic era. Annu. Rev. Genomics Hum. Genet. 15, 417–441 (2014).

    CAS  PubMed  Google Scholar 

  • 74.

    Kess, T., Galindo, J. & Boulding, E. G. Genomic divergence between Spanish Littorina saxatilis ecotypes unravels limited admixture and extensive parallelism associated with population history. Int. J. Bus. Innov. Res. 17, 8311–8327 (2018).

    Google Scholar 

  • 75.

    Bohutínská, M. et al. Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives. Preprint at BioRxiv https://doi.org/10.1101/2020.03.24.005397 (2020).

  • 76.

    Rennison, D. J., Samuk, K., Owens, G. L. & Miller, S. E. Shared patterns of genome-wide differentiation are more strongly predicted by geography than by ecology. Am. Nat. 195, 192–200 (2019).

    PubMed  Google Scholar 

  • 77.

    Lucek, K., Sivasundar, A., Roy, D. & Seehausen, O. Repeated and predictable patterns of ecotypic differentiation during a biological invasion: lake–stream divergence in parapatric Swiss stickleback. J. Evol. Biol. 26, 2691–2709 (2013).

    CAS  PubMed  Google Scholar 

  • 78.

    Berner, D., Roesti, M., Hendry, A. P. & Salzburger, W. Constraints on speciation suggested by comparing lake–stream stickleback divergence across two continents. Mol. Ecol. 19, 4963–4978 (2010).

    PubMed  Google Scholar 

  • 79.

    Giles, N. Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus L. Anim. Behav. 31, 1192–1194 (1983).

    Google Scholar 

  • 80.

    Spence, R., Wootton, R. J., Barber, I., Przybylski, M. & Smith, C. Ecological causes of morphological evolution in the three-spined stickleback. Ecol. Evol. 3, 1717–1726 (2013).

    PubMed  PubMed Central  Google Scholar 

  • 81.

    Reimchen, T. E. Incidence and intensity of Cyathocephalus truncatus and Schistocephalus solidus infection in Gasterosteus aculeatus. Can. J. Zool. 60, 1091–1095 (1982).

    Google Scholar 

  • 82.

    MacColl, A. D. C. Parasite burdens differ between sympatric three-spined stickleback species. Ecography 32, 153–160 (2009).

    Google Scholar 

  • 83.

    Stutz, W. E., Lau, O. L. & Bolnick, D. I. Contrasting patterns of phenotype-dependent parasitism within and among populations of threespine stickleback. Am. Nat. 183, 810–825 (2014).

    PubMed  Google Scholar 

  • 84.

    Bassham, S., Catchen, J., Lescak, E., von Hippel, F. A. & Cresko, W. A. Repeated selection of alternatively adapted haplotypes creates sweeping genomic remodeling in stickleback. Genetics 209, 921–939 (2018).

    PubMed  PubMed Central  Google Scholar 

  • 85.

    Etter, P. D., Preston, J. L., Bassham, S., Cresko, W. A. & Johnson, E. A. Local de novo assembly of RAD paired-end contigs using short sequencing reads. PLoS ONE 6, e18561 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 86.

    Ali, O. A. et al. Rad capture (Rapture): flexible and efficient sequence-based genotyping. Genetics 202, 389–400 (2016).

    CAS  PubMed  Google Scholar 

  • 87.

    Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).

    PubMed  PubMed Central  Google Scholar 

  • 88.

    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    CAS  Google Scholar 

  • 89.

    Chang, C. C. et al. Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience 4, 7 (2015).

    PubMed  PubMed Central  Google Scholar 

  • 90.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017); https://www.R-project.org/

  • 91.

    Günther, T. & Coop, G. Robust identification of local adaptation from allele frequencies. Genetics 195, 205–220 (2013).

    PubMed  PubMed Central  Google Scholar 

  • 92.

    Yeaman, S. et al. Convergent local adaptation to climate in distantly related conifers. Science 353, 1431–1433 (2016).

    CAS  PubMed  Google Scholar 

  • 93.

    Storey, J. qvalue: Q-value estimation for false discovery rate control. R package version 2.0.0 (2015).

  • 94.

    Pfeifer, B., Wittelsbürger, U., Ramos-Onsins, S. E. & Lercher, M. J. PopGenome: an efficient Swiss Army knife for population genomic analyses in R. Mol. Biol. Evol. 31, 1929–1936 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 


  • Source: Ecology - nature.com

    Continuous moulting by Antarctic krill drives major pulses of carbon export in the north Scotia Sea, Southern Ocean

    An escape route for seafloor methane