CHROMOSOME INVERSIONS, ADAPTIVE CASSETTES AND THE EVOLUTION OF SPECIES’ RANGES
Mark Kirkpatrick
Department of Integrative Biology, University of Texas, Austin, TX, 78712 USA
Search for more papers by this authorBrian Barrett
Department of Integrative Biology, University of Texas, Austin, TX, 78712 USA
Search for more papers by this authorMark Kirkpatrick
Department of Integrative Biology, University of Texas, Austin, TX, 78712 USA
Search for more papers by this authorBrian Barrett
Department of Integrative Biology, University of Texas, Austin, TX, 78712 USA
Search for more papers by this authorSpencer C. H. Barrett
Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON, M5S 3B2 Canada
Search for more papers by this authorRobert I. Colautti
Department of Biology, Queen's University, Kingston, ON, K7L 3N6 Canada
Search for more papers by this authorKatrina M. Dlugosch
Department of Ecology and Evolutionary Biology, University of Arizona, PO Box 210088, Tucson, AZ, 85721 USA
Search for more papers by this authorLoren H. Rieseberg
Department of Botany, University of British Columbia, 1316–6270 University Blvd., Vancouver, BC, V6T 1Z4 Canada
Department of Biology, Indiana University, Bloomington, IN, 47405 USA
Search for more papers by this authorSummary
A chromosome inversion can spread when it captures locally adapted alleles or when it is introduced into a species by hybridization with adapted alleles that were previously absent. We present a model that shows how both processes can cause a species range to expand. Introgression of an inversion that carries novel, locally adapted alleles is a particularly powerful mechanism for range expansion. The model supports the earlier proposal that introgression of an inversion triggered a large range expansion of a malaria mosquito. These results suggest a role for inversions as cassettes of genes that can accelerate adaptation by crossing species boundaries, rather than protecting genomes from introgression.
REFERENCES
- Alleaume-Benharira M, Pen IR, Ronce O (2006) Geographical patterns of adaptation within a species' range: interactions between drift and gene flow. Journal of Evolutionary Biology, 19, 203–215.
- Atkins KE, Travis JMJ (2010) Local adaptation and the evolution of species' ranges under climate change. Journal of Theoretical Biology, 266, 449–457.
- Ayala FJ, Coluzzi M (2005) Chromosome speciation: humans, Drosophila, and mosquitoes. Proceedings of the National Academy of Sciences of the United States of America, 102, 6535–6542.
- Ayala D, Guerrero RF, Kirkpatrick M (2012) Reproductive isolation and local adaptation quantified for a chromosome inversion in a malaria mosquito. Evolution, 67, 946–958.
- Ayala D, Ullastres A, González J (2014) Adaptation through chromosomal inversions in Anopheles. Frontiers in Genetics, 5, 129.
- Barton NH (2001) Adaptation at the edge of a species' range. In: Integrating Ecology and Evolution in a Spatial Context (eds J Silvertown, J Antonovics), pp. 365–392. Blackwell, Oxford.
- Behrman KD, Kirkpatrick M (2011) Species range expansion by beneficial mutations. Journal of Evolutionary Biology, 24, 665–675.
- Besansky NJ, Krzywinski J, Lehmann T et al. (2003) Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation. Proceedings of the National Academy of Sciences of the United States of America, 100, 10818–10823.
- Bourne EC, Bocedi G, Travis JMJ et al. (2014) Between migration load and evolutionary rescue: dispersal, adaptation and the response of spatially structured populations to environmental change. Proceedings of the Royal Society B-Biological Sciences, 281, 20132795.
- Bridle JR, Polechova J, Kawata M, Butlin RK (2010) Why is adaptation prevented at ecological margins? New insights from individual-based simulations. Ecology Letters, 13, 485–494.
- Case TJ, Taper ML (2000) Interspecific competition, environmental gradients, gene flow, and the coevolution of species' borders. American Naturalist, 155, 583–605.
- Charlesworth B, Coyne JA, Barton NH (1987) The relative rates of evolution of sex-chromosomes and autosomes. American Naturalist, 130, 113–146.
- Cheng L (1985) Biology of Halobates (Heteroptera: Gerridae). Annual Review of Entomology, 30, 111–135.
- Darmon E, Leach DRF (2014) Bacterial genome instability. Microbiology and Molecular Biology Reviews, 78, 1–39.
- Duputie A, Massol F, Chuine I, Kirkpatrick M, Ronce O (2012) How do genetic correlations affect species range shifts in a changing environment? Ecology Letters, 15, 251–259.
- Filin I, Holt RD, Barfield M (2008) The relation of density regulation to habitat specialization, evolution of a species' range, and the dynamics of biological invasions. American Naturalist, 172, 233–247.
- Fishman L, Stathos A, Beardsley PM, Williams CF, Hill JP (2013) Chromosomal rearrangements and the genetics of reproductive barriers in Mimulus (monkeyflowers). Evolution, 67, 2547–2560.
- Fouet C, Gray E, Besansky NJ, Costantini C (2012) Adaptation to aridity in the malaria mosquito Anopheles gambiae: chromosomal inversion polymorphism and body size influence resistance to desiccation. PLoS ONE, 7, e34841.
- Garcia-Ramos G, Rodriguez D (2002) Evolutionary speed of species invasions. Evolution, 56, 661–668.
- Gaston KJ (2003) The Structure and Dynamics of Geographic Ranges. Oxford University Press, Oxford.
- Goldberg EE, Lande R (2006) Ecological and reproductive character displacement on an environmental gradient. Evolution, 60, 1344–1357.
- Goldberg EE, Lande R (2007) Species' borders and dispersal barriers. American Naturalist, 170, 297–304.
- Gomulkiewicz R, Holt RD, Barfield M (1999) The effects of density dependence and immigration on local adaptation and niche evolution in a black-hole sink environment. Theoretical Population Biology, 55, 283–296.
- Haldane JBS (1956) The relation between density regulation and natural selection. Proceedings of the Royal Society Series B-Biological Sciences, 145, 306–308.
- Hoffmann AA, Rieseberg LH (2008) Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annual Review of Ecology Evolution and Systematics, 39, 21–42.
- Holt RD, Barfield M, Filin I, Forde S (2011) Predation and the evolutionary dynamics of species ranges. American Naturalist, 178, 488–500.
- Jones FC, Grabherr MG, Chan YF et al. (2012) The genomic basis of adaptive evolution in threespine sticklebacks. Nature, 484, 55–61.
- Joron M, Frezal L, Jones RT et al. (2011) Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature, 477, 203–U102.
- Kirkpatrick M (2010) How and why chromosome inversions evolve. Plos Biology, 8, e1000501.
- Kirkpatrick M, Barton NH (1997) Evolution of a species' range. American Naturalist, 150, 1–23.
- Kirkpatrick M, Barton N (2006) Chromosome inversions, local adaptation, and speciation. Genetics, 173, 419–434.
- Kirkpatrick M, Peischl S (2013) Evolutionary rescue by beneficial mutations in environments that change in space and time. Philosophical Transactions of The Royal Society B-Biological Sciences, 368, 20120082.
- Lande R (1979) Effective deme sizes during long-term evolution estimated from rates of chromosomal rearrangement. Evolution, 33, 234–251.
- Lande R (1985) The fixation of chromosomal rearrangements in a subdivided population with local extinction and colonization. Heredity, 54, 323–332.
- Lewontin RC, Birch LC (1966) Hybridization as a source of variation for adaptation to new environments. Evolution, 20, 315–336.
- Lowry DB, Willis JH (2010) A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. Plos Biology, 8, e1000500.
-
Mayr E (1963) Animal Species and Evolution. Harvard University Press, Cambridge.
10.1111/j.0022-1112.2004.00433.x Google Scholar
- Misof B, Liu S, Meusemann K et al. (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science, 346, 763–767.
- Navarro A, Barton NH (2003) Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution, 57, 447–459.
- Noor MAF, Grams KL, Bertucci LA, Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. Proceedings of the National Academy of Sciences of the United States of America, 98, 12084–12088.
- Nosil P, Feder JL (2013) Genome evolution and speciation: toward quantitative descriptions of pattern and process. Evolution, 67, 2461–2467.
- Nuismer SL, Kirkpatrick M (2003) Gene flow and the coevolution of parasite range. Evolution, 57, 746–754.
- Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299–304.
- Oneal E, Lowry DB, Wright KM, Zhu ZR, Willis JH (2014) Divergent population structure and climate associations of a chromosomal inversion polymorphism across the Mimulus guttatus species complex. Molecular Ecology, 23, 2844–2860.
- Pease CP, Lande R, Bull JJ (1989) A model of population growth, dispersal and evolution in a changing environment. Ecology, 70, 1657–1664.
- Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends in Ecology & Evolution, 16, 351–358.
- Ronce O, Kirkpatrick M (2001) When sources become sinks: migrational meltdown in heterogeneous habitats. Evolution, 55, 1520–1531.
- Sexton JP, McIntyre PJ, Angert AL, Rice KJ (2009) Evolution and ecology of species range limits. Annual Review of Ecology Evolution and Systematics, 40, 415–436.
- Sharakhov IV, White BJ, Sharakhova MV et al. (2006) Breakpoint structure reveals the unique origin of an interspecific chromosomal inversion (2La) in the Anopheles gambiae complex. Proceedings of the National Academy of Sciences of the United States of America, 103, 6258–6262.
- Slatkin M (1973) Gene flow and selection in a cline. Genetics, 75, 733–756.
- Tsutsui ND, Suarez AV (2003) The colony structure and population biology of invasive ants. Conservation Biology, 17, 48–58.
- Turner JRG, Wong HY (2010) Why do species have a skin? Investigating mutational constraint with a fundamental population model. Biological Journal of the Linnean Society, 101, 213–227.
- Wallace B (1975) Hard and soft selection revisited. Evolution, 29, 465–473.
- Wang J, Wurm Y, Nipitwattanaphon M et al. (2013) A Y-like social chromosome causes alternative colony organization in fire ants. Nature, 493, 664–668.
- White BJ, Hahn MW, Pombi M et al. (2007) Localization of candidate regions maintaining a common polymorphic inversion (2La) in Anopheles gambiae . Plos Genetics, 3, 2404–2414.
- White BJ, Cheng CD, Sangare D et al. (2009) The population genomics of trans-specific inversion polymorphisms in Anopheles gambiae . Genetics, 183, 275–288.
- White BJ, Collins FH, Besansky NJ (2011) Evolution of Anopheles gambiae in relation to humans and malaria. Annual Review of Ecology, Evolution, and Systematics, 42, 111–132.
- Wolfram_Research (2014) Mathematica 10.0, 10.0 edn. Wolfram Research, Champaign, Illinois.
- Yeaman S, Whitlock MC (2011) The genetic architecture of adaptation under migration-selection balance. Evolution, 65, 1897–1911.
- Zhang Z-Q (2011) Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa, 3148, 7–12.