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How and Why Chromosome Inversions Evolve

  • Mark Kirkpatrick mail

    kirkp@mail.utexas.edu

    Affiliation: Section of Integrative Biology, University of Texas, Austin, Texas, United States of America

    X
  • Published: September 28, 2010
  • DOI: 10.1371/journal.pbio.1000501

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Comment on the article by Kirkpatrick ‘How and Why Chromosome Inversions Evolve’

Posted by mmatos on 30 Sep 2010 at 20:05 GMT

Margarida Matos
Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Campo Grande 1749-016 Lisboa, Portugal
Email: mmatos@fc.ul.pt

Kirkpatrick’s article on the evolution of chromosome inversions (1) is a welcome review on a topic that is intriguing evolutionary biologists for more than 70 years, starting with Dobzhansky’s detailed analysis of temporal and spacial changes in frequencies of chromosomal inversions suggestion the role of both natural selection and genetic drift (2). In a sense it may seem thus surprising that we are still struggling to understand why inversions are selected, e.g. due to complex gene complexes or local adaptation preserved by reduced recombination between close populations (3, 4). Some of the most interesting data that reinforces the role of natural selection are geographical clines, in particular consistent changes in frequency of specific genic rearrangements with latitude. Empirical evidence associating specific inversions with particular latitudes, leading to consistent genetic differentiation between populations even in the presence of gene flux clearly suggest that natural selection plays a role through local adaptation, whichever the particular genetic basis and evolutionary mechanism involved. Clearly one environmental factor that may be involved is temperature, whether directly or indirectly, by its impact in the abiotic and biotic features of the environment. Empirical data are essential to reinforce the general evolutionary interpretation of inversion polymorphism and specific mechanisms involve different expectations (3, 4, 5). Kirkpatrick picked one such example, latitudinal clines involving two gene arrangements in Drosophila melanogaster that appear in three different continents (6) This is thus a powerful evidence, in that it is repeatable, reducing the limitations of a single cline that might be shaped by misleading forces, history included. Moreover it has been shown that inversions are changing as expected by climate warning (7). In spite my appreciation of these set of data, I was surprised that Kirkpatrick did not mention even stronger evidences of the role of natural selection shaping latitudinal clines in the studies in Drosophila subobscura (a highly polymorphic species for inversions) that involve real time evolution analysis after the colonization of South and North America from an European source, in the 70s-80s (8). In a long time-series study it has been shown that as populations spread along the coast of South and North America, latitudinal clines were defined in the same general direction as the much older European cline (9). Moreover recent data also show clear indications of changes as expected due to climate change (10) This set of data are unique in being the first natural experimental evolution study (that is, seen in real time) with replication. I regret that Kirkpatrick did not mention these works, as they strongly build in a more solid background for future dissection about the genetic basis of local adaptation involved in latitudinal clines and, through this, about the evolutionary dynamics of inversions in general.
References
1 – Kirkpatrick M 2010. ‘How and Why Chromosome Inversions Evolve’. PloS Biology 8 (9). e1000501.
2 - Lewontin RC, Moore JA, Provine WB, Wallace B (eds.) (1981). Dobzhansky's Genetics of Natural Populations I-XLIII. Columbia University Press, New York.
3 - Kirkpatrick M, Barton N (2006) Chromosome inversions, local adaptation, and
speciation. Genetics 173: 419–434.
4 – Hoffmann, A, Rieseberg LH (2008). Revisiting the Impact of Inversions in Evolution: From Population Genetic Markers to Drivers of Adaptive Shifts and Speciation? Annu. Rev. Ecol. Evol. Syst. 2008. 39:21–42
5 - Santos, M. 2009. Recombination load in a chromosomal inversion polymorphism of Drosophila subobscura. Genetics 181:803-809.
6 - Krimbas CB, Powell JR (1992) Drosophila inversion polymorphism. London: CRC Press.
7 - Anderson AR, Hoffmann AA, McKechnie SW, Umina PA, Weeks AR (2005) The latitudinal cline in the In(3R)Payne inversion polymorphism has shifted in the last 20 years in Australian Drosophila melanogaster populations. Mol Ecol 14: 851–858.
8 - Pascual, M, Chapuis MP, Mestres F, Balanyà J., Huey RB, Gilchrist GW, Serra L, Estoup A 2007. Introduction history of Drosophila subobscura in the new world: a microsatellite-based survey using abc methods. Mol. Ecol. 16: 3069–3083.
9 - Balanyà J, Serra L, Gilchrist GW, Huey RB, Pascual M, Mestres F, Solé E 2003. Evolutionary pace of chromosomal polymorphism in colonizing populations of Drosophila subobscura: an evolutionary time series. Evolution 57: 1837–1845.
10 - Balanyà J, Oller JM, Huey RB, Gilchrist GW, Serra L (2006). Global Genetic Change Tracks Global Warming in Drosophila subobscura. Science. 313: 1773-1775.

No competing interests declared.

RE: Comment on the article by Kirkpatrick ‘How and Why Chromosome Inversions Evolve’

kirkp replied to mmatos on 21 Apr 2014 at 18:03 GMT

I am happy that Matos draws attention to the beautiful work on inversion clines in Drosophila subobscura. Space constraints prevented me from citing this and other important cases, and it's great that this comment will expand people's awareness of this literature.

No competing interests declared.