COMMENTARY The way the world might be

Theoreticians are interested in the way the world might be, seeking theories of ‘elegant and economical...mathematical form, in the expectation that they will prove the ones realized in nature’ (Polkinghorne, 1983, p. 9–10). Empiricists, on the contrary, prefer to know ‘The Way the World Is’ (as in Polkinghorne’s title). Ideally, our understanding advances by an interplay between the two. As Darwin insisted ‘all observation must be for or against some view if it is to be of any service!’ (see Browne, 2002, p. 56): gathering of experimental and observational data without a guiding theoretical framework is generally not productive. A good guide to the value of new theory, therefore, should be its impact on the course of empirical work and, conversely, new theory should be firmly grounded in the existing body of data. How does Adaptive Dynamics fare in this context? We were struck by the fact that Waxman & Gavrilets’ (2004) review contains only a single reference to an empirical study amongst its 90 or so citations. They are critical of the Adaptive Dynamics approach primarily on theoretical grounds, challenging one view of how the world might be with other views of how it might be, rather than confronting the theory with the way the world actually is. The empiricist encountering Waxman and Gavrilets’ Section 4 on the major assumptions of Adaptive Dynamics might have expected to see these assumptions compared with data. There are data available on the sizes of allelic effects and on the numbers of loci contributing to standing genetic variation (e.g. Hayes & Goddard, 2001; Mackay, 2001) or the differences between species in quantitative traits (Orr, 2001), on the prevalence of dominance and epistasis (e.g. Lukens & Doebley, 1999) and on effective population sizes (and hence drift) (e.g. Frankham, 1995). The Adaptive Dynamics assumptions do not fit easily into this body of information: genetic variation in quantitative traits within populations is almost ubiquitous, mutations of large effect do occur with appreciable frequency, departures from additivity are widespread and effective population sizes are often small. Of course, models must make simplifying assumptions, so how do we judge what Waxman and Gavrilets call ‘the consequences of violation’? Surely, the answer must be to compare the predictions of models with empirical observations. Ideally, one would do this in simple and well-understood situations before going on to make predictions about more complex problems where discrepancies may have many different explanations (like sympatric speciation, see below). Population genetics theory provides good predictions of the outcome of both selection and drift in controlled laboratory experiments and simple natural situations, like the evolution of insecticide resistance (Taylor, 1986). The same is true for game theory (e.g. dung fly waiting times: Parker, 1970). Can similar tests be devised for Adaptive Dynamics? We strongly support the call by Waxman and Gavrilets (Section 6) for comparisons between model predictions and empirical data but we see no clear guidance for empiricists on the critical data they need to collect, either in the Adaptive Dynamics literature or in Waxman and Gavrilets’ review. Adaptive Dynamics came to the attention of many evolutionary biologists through the sympatric speciation model of Dieckmann & Doebeli (1999) (hereafter DD99). Waxman and Gavrilets are critical of this contribution on several counts (Sections 5.2 & 5.3). Whatever the merits of these arguments, it is clear that a complex model, building on a long history of theoretical development and claiming to arrive at a different conclusion, should not be accepted without careful examination. We have investigated the impact of DD99 on views of sympatric speciation as an example of the interplay between theoretical and empirical approaches in evolutionary biology. A search of the ISI Science Citation Index (Expanded) on 5 April 2004 revealed 200 citations of DD99. The original paper was published in a well-known weekly magazine, Nature, whose extremely condensed format makes it very difficult to provide adequate detail, for example about the assumptions inherent in a simulation model. Dieckmann and Doebeli expanded their arguments and provided a more extensive discussion in a subsequent paper (Doebeli & Dieckmann, 2000) but this has only been cited 39 times. Abrams (2001) compared the Adaptive Dynamics approach with population genetic and game theory approaches. He questioned the assumption in DD99 that there is no cost to assortative mating and considered the effectiveness of mate selection in the model to be unrealistically high. Abrams’ paper has been cited only 12 times. Similarly, Day (2001) pointed out that population structure reduces the tendency towards evolutionary branching and is absent in the DD99 model. Waxman and Gavrilets note the ubiquity of population structure (Section 5.3), although they draw different implications. Day’s paper has been cited only three times compared with over 100 citations in the same time post-publication for DD99. We classified papers citing DD99 according to the type of contribution (empirical, theoretical or review/comment) and on whether nonallopatric speciation was a central issue in the paper or not (Table 1). We then looked at the way DD99 was reported: was it quoted as evidence that nonallopatric speciation is now considered Correspondence: Roger K. Butlin, Department of Animal and Plant Sciences, The University of Sheffield, Sheffield S10 2TN, UK. Tel.: +44 (0)114 222 0097; fax: +44 (0)114 222 0002; e-mail: [email protected]