Behavior

Biological Journal of the Linnean Society, 2008, 95, 26–46. With 6 figures

A Century of Evolution: Ernst Mayr (1904–2005) Ernst Mayr and the integration of geographic and ecological factors in speciation
PATRIK NOSIL*
Zoology Department and Biodiversity Research Centre, University of British Columbia, Vancouver BC, V6T 1Z4, Canada
Received 3 February 2008; accepted for publication 22 May2008

Mayr’s best recognized scientific contributions include the biological species concept and the theory of geographic speciation. In the latter, reproductive isolation evolves as an incidental by-product of genetic divergence between allopatric populations. Mayr noted that divergent natural selection could accelerate speciation, but also argued that gene flow so strongly retards divergence that,even with selection, non-allopatric speciation is unlikely. However, current theory and data demonstrate that substantial divergence, and even speciation, in the face of gene flow is possible. Here, I attempt to connect some opposing views about speciation by integrating Mayr’s ideas about the roles of ecology and geography in speciation with current data and theory. My central premise is that thespeciation process (i.e. divergence) is often continuous, and that the opposing processes of selection and gene flow interact to determine the degree of divergence (i.e. the degree of progress towards the completion of speciation). I first establish that, in the absence of gene flow, divergent selection often promotes speciation. I then discuss how population differentiation in the face of gene flowis common when divergent selection occurs. However, such population differentiation does not always lead to the evolution of discontinuities, strong reproductive isolation, and thus speciation per se. I therefore explore the genetic and ecological circumstances that facilitate speciation in the face of gene flow. For example, particular genetic architectures or ecological niches may tip the balancebetween selection and gene flow strongly in favour of selection. The circumstances allowing selection to overcome gene flow to the extent that a discontinuity develops, and how often these circumstances occur, are major remaining questions in speciation research. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95, 26–46.

ADDITIONAL KEYWORDS: divergentnatural selection – gene flow – niche dimensionality – reproductive
isolation – sympatric speciation – Timema walking-stick insects.

INTRODUCTION
Ernst Mayr made numerous contributions to speciation research from conceptual, systematic, genetic, and ecological perspectives. His greatest conceptual influence comes from the popularization of the biological species concept (BSC), which considers speciesas groups of actually or potentially interbreeding natural populations that are reproductively isolated from other such groups (Mayr, 1942). Elements of the BSC had been noted before Mayr (Wallace, 1864; Dobzhansky, 1935, 1937; Haffer, 2006), but Mayr
*E-mail: pnosil@zoology.ubc.ca

spread and crystallized the idea that the evolution of reproductive isolation is an essential component ofspeciation. Another well-recognized contribution is the theory of geographic speciation, whereby genetic divergence between geographically-separated (allopatric) populations results in speciation. Under this scenario, gene flow between populations prevents the evolution of reproductive isolation, most speciation is allopatric, and speciation in the face of gene flow is considered rare, if it occurs atall. Although this is probably still the dominant view among biologists, current theory and data demonstrate that substantial divergence, and even speciation, in the face of gene flow is possible (Turelli, Barton & Coyne, 2001; Via,

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© 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95, 26–46

MAYR AND ECOLOGICAL SPECIATION 2001; Berlocher & Feder,...