The coupling hypothesis: why genome scans may fail to map local adaptation genes.
Nicolas Bierne,Nicolas Bierne,John J. Welch,Etienne Loire,François Bonhomme,François Bonhomme,Patrice David,Patrice David +7 more
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TLDR
It is argued that endogenous genetic barriers are often more likely than local adaptation to explain the majority of Fst‐outlying loci observed in genome scan approaches – even when these are correlated to environmental variables.Abstract:
Genomic scans of multiple populations often reveal marker loci with greatly increased differentiation between populations. Often this differentiation coincides in space with contrasts in ecological factors, forming a genetic–environment association (GEA). GEAs imply a role for local adaptation, and so it is tempting to conclude that the strongly differentiated markers are themselves under ecologically based divergent selection, or are closely linked to loci under such selection. Here, we highlight an alternative and neglected explanation: intrinsic (i.e. environment-independent) pre- or post-zygotic genetic incompatibilities rather than local adaptation can be responsible for increased differentiation. Intrinsic genetic incompatibilities create endogenous barriers to gene flow, also known as tension zones, whose location can shift over time. However, tension zones have a tendency to become trapped by, and therefore to coincide with, exogenous barriers due to ecological selection. This coupling of endogenous and exogenous barriers can occur easily in spatially subdivided populations, even if the loci involved are unlinked. The result is that local adaptation explains where genetic breaks are positioned, but not necessarily their existence, which can be best explained by endogenous incompatibilities. More precisely, we show that (i) the coupling of endogenous and exogenous barriers can easily occur even when ecological selection is weak; (ii) when environmental heterogeneity is fine-grained, GEAs can emerge at incompatibility loci, but only locally, in places where habitats and gene pools are sufficiently intermingled to maintain linkage disequilibria between genetic incompatibilities, local-adaptation genes and neutral loci. Furthermore, the association between the locally adapted and intrinsically incompatible alleles (i.e. the sign of linkage disequilibrium between endogenous and exogenous loci) is arbitrary and can form in either direction. Reviewing results from the literature, we find that many predictions of our model are supported, including endogenous genetic barriers that coincide with environmental boundaries, local GEA in mosaic hybrid zones, and inverted or modified GEAs at distant locations. We argue that endogenous genetic barriers are often more likely than local adaptation to explain the majority of Fst-outlying loci observed in genome scan approaches – even when these are correlated to environmental variables. (Resume d'auteur)read more
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Hybridization and speciation
Richard J. Abbott,Dirk C. Albach,Stephen W. Ansell,Jan W. Arntzen,Stuart J. E. Baird,Nicolas Bierne,Janette W. Boughman,Alan Brelsford,C. A. Buerkle,Richard J. A. Buggs,Roger K. Butlin,Ulf Dieckmann,Fabrice Eroukhmanoff,Andrea Grill,Sara Helms Cahan,Jo S. Hermansen,Godfrey M. Hewitt,Alan G. Hudson,Chris D. Jiggins,Julia C. Jones,Barbara Keller,T. Marczewski,James Mallet,Paloma Martínez-Rodríguez,Markus Möst,Sean P. Mullen,Richard A. Nichols,Arne W. Nolte,Christian Parisod,Karin S. Pfennig,Amber M. Rice,Michael G. Ritchie,Burkhardt Seifert,Carole M. Smadja,Rike B. Stelkens,Jacek M. Szymura,Risto Väinölä,Jochen B. W. Wolf,Dietmar Zinner +38 more
TL;DR: A perspective on the context and evolutionary significance of hybridization during speciation is offered, highlighting issues of current interest and debate and suggesting that the Dobzhansky–Muller model of hybrid incompatibilities requires a broader interpretation.
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Genomics and the origin of species
Ole Seehausen,Roger K. Butlin,Irene Keller,Catherine E. Wagner,Janette W. Boughman,Paul A. Hohenlohe,Catherine L. Peichel,Glenn-Peter Sætre,Claudia Bank,Åke Brännström,Alan Brelsford,Chris S Clarkson,Fabrice Eroukhmanoff,Jeffrey L. Feder,Martin C. Fischer,Andrew D. Foote,Paolo Franchini,Chris D. Jiggins,Felicity C. Jones,Anna K. Lindholm,Kay Lucek,Martine E. Maan,David Alexander Marques,Simon H. Martin,Blake Matthews,Joana I. Meier,Markus Möst,Michael W. Nachman,Etsuko Nonaka,Diana J. Rennison,Julia Schwarzer,E. Watson,Anja M. Westram,Alex Widmer +33 more
TL;DR: Emergent trends and gaps in understanding are identified, new approaches to more fully integrate genomics into speciation research are proposed, and an integrative definition of the field of speciation genomics is provided.
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Wonderful Life: The Burgess Shale and the Nature of History, Stephen Jay Gould. W. W. Norton, New York (1989), 347, Price $19.95 (U.S.A.), $27.95 (Canada)
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The relative power of genome scans to detect local adaptation depends on sampling design and statistical method
TL;DR: This work compares FST outlier and genetic–environment association (GEA) methods for each of two approaches that control for population structure: with a covariance matrix or with latent factors and shows that while the relative power of two methods in the same category depended largely on the number of individuals sampled, overall GEA tests had higher power in the island model and FST had higherPower under isolation by distance.
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