ARE SPECIES REAL? THE SHAPE OF THE SPECIES BOUNDARY WITH EXPONENTIAL FAILURE, REINFORCEMENT, AND THE “MISSING SNOWBALL”

Authors

  • Sébastien Gourbière,

    1. UMR 5244 CNRS-EPHE-UPVD, Laboratoire de Biologie et d’Ecologie Tropicale et Méditerranéenne, Université de Perpignan, Via Domitia, 52 Avenue Paul Alduy, 66 860 Perpignan Cedex, France
    2. E-mail: gourbier@univ-perp.fr
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  • James Mallet

    1. Wissenschaftskolleg zu Berlin, Wallotstraße 19, 14193 Berlin, Germany
    2. Galton Laboratory, Department of Genetics, Evolution and Environment, University College London, 4 Stephenson Way, London NW1 2HE, United Kingdom
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Abstract

Under simple assumptions, the evolution of epistatic “Dobzhansky–Muller” incompatibilities between a pair of species should yield an accelerating decline of log overall reproductive compatibility—a “snowball” effect that might rapidly provide new species with “reality.” Possible alternatives include: (1) simple exponential failure, giving a linear rate of log compatibility loss, and (2) “slowdown,” likely during reinforcement in which mate choice evolves to prevent deleterious hybridization, yielding a decelerating log compatibility loss. In analyses of multiple datasets, we find little support for the snowball effect, except possibly in Lepidoptera hybrid viability. The snowball predicts a slow initial rate of incompatibility acquisition, with low initial variance; instead, highly variable compatibility is almost universally observed at low genetic distances. Another deviation from predictions is that reproductive isolation usually remains incomplete until long after speciation. These results do not disprove snowball compatibility decay, but can result if large deleterious effects are due to relatively few genetic changes, or if different types of incompatibility evolve at very different rates. On the other hand, data on Bacillus and Saccharomyces, as well as theories of chromosomal evolution, suggest that some kinds of incompatibility accumulate approximately linearly, without Dobzhansky–Muller effects. In microorganisms, linearity can result from direct negative effects of DNA sequence divergence on compatibility. Finally, a decelerating slowdown model is supported for sympatric Leptasterias starfish, and in Drosophila prezygotic isolation in sympatry but not allopatry, providing novel comparative evidence for reinforcement.

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