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Genes versus phenotypes in the study of speciation

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Abstract

Despite persistent debate on the nature of species, the widespread adoption of Mayr’s biological species concept has led to a heavy emphasis on the importance of reproductive isolation to the speciation process. Equating the origin of species with the evolution of reproductive isolation has become common practice in the study of speciation, coincident with an increasing focus on elucidating the specific genetic changes (i.e.—speciation genes) underlying intrinsic reproductive barriers between species. In contrast, some have recognized that reproductive isolation is usually a signature effect rather than a primary cause of speciation. Here we describe a research paradigm that shifts emphasis from effects to causes in order to resolve this apparent contradiction and galvanize the study of speciation. We identify major elements necessary for a balanced and comprehensive investigation of the origin of species and place the study of so-called “speciation genes” into its appropriate context. We emphasize the importance of characterizing diverging phenotypes, identifying relevant evolutionary forces acting on those phenotypes and their role in the causal origins of reduced gene flow between incipient species, and the nature of the genetic and phenotypic boundaries that results from such processes. This approach has the potential to unify the field of speciation research, by allowing us to make better “historical” predictions about the fate of diverging populations regardless of taxon.

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Acknowledgments

This manuscript was invited as part of a recent symposium organized to honor Richard G. Harrison’s contribution to the field of evolutionary genetics. We thank Rick for many in-depth discussions on the topic of speciation and for providing an intellectually stimulating environment within which to work. We also thank Ben Normark, Daniel Howard, and David Rand for their efforts organizing the symposium as well as members of the Shaw and Mullen labs for feedback on the topic of this paper. We also thank two anonymous reviewers, J. Hebert and D. Baldassarre for comments on a previous draft.

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Correspondence to Kerry L. Shaw.

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Kerry L. Shaw and Sean P. Mullen contributed equally to this work.

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Shaw, K.L., Mullen, S.P. Genes versus phenotypes in the study of speciation. Genetica 139, 649–661 (2011). https://doi.org/10.1007/s10709-011-9562-4

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