Disruptive selection and then what?

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Disruptive selection occurs when extreme phenotypes have a fitness advantage over more intermediate phenotypes. The phenomenon is particularly interesting when selection keeps a population in a disruptive regime. This can lead to increased phenotypic variation while disruptive selection itself is diminished or eliminated. Here, we review processes that increase phenotypic variation in response to disruptive selection and discuss some of the possible outcomes, such as sympatric species pairs, sexual dimorphisms, phenotypic plasticity and altered community assemblages. We also identify factors influencing the likelihoods of these different outcomes.

Introduction

A population experiences disruptive selection (see Glossary) on a quantitative trait when intermediate phenotypes have a fitness disadvantage compared with more extreme phenotypes. During the 1950s and 1960s, disruptive selection figured prominently in mainstream evolutionary thinking, with the realization that it might have several consequences for the evolution of phenotypic variability 1, 2, 3, 4, 5, 6, including the maintenance of high levels of genetic variation, sympatric speciation, the emergence of allelic switches between alternative phenotypes and the evolution of phenotypic plasticity. After a period of diminished interest in the idea 7, 8, renewed attempts at understanding disruptive selection were made during the 1990s 9, 10, 11, 12, 13. An important new insight was that two types of disruptive selection must be distinguished, of which only one has a diversifying effect (Box 1).

For disruptive selection to occur, the mean phenotype has to experience the lowest fitness. In the first type, which does not lead to diversification, selection prevents a population from experiencing such a situation for any significant amount of time. Instead, the population evolves away from the region of disruptive selection (Box 1, Figure Ia). For example, imagine a situation where a consumer feeds on two resources, say, large and small seeds, whose abundance is maintained at relatively constant levels by other factors. Consumers with intermediate phenotypes perform poorly on both resources and have a smaller energy intake rate than do either of the more extreme phenotypes. Thus, directional selection acts towards specialization in the direction of the closer fitness peak.

For the second type of disruptive selection, we can imagine a situation where a population exploits a continuously varying resource, such as seeds that range from very small to very large and where the level of consumption influences seed abundance. Individuals that efficiently exploit the most abundant resource (e.g. seeds of intermediate size) have a fitness advantage and the mean of the population will move towards this optimum (Figure 1a). Once most of the population is specialized on the most abundant resource, this part of the resource spectrum is depleted, and that phenotype is no longer favored (Figure 1b). As a result, phenotypes that deviate from the most common type have a fitness advantage and the population experiences disruptive selection. This is maintained until phenotypic variation increases to the point where the available resource spectrum is used more equally (Box 1 Figure Ic). This scenario is driven by negative frequency-dependent selection, emerging from competition for resources. Rare types enjoy an advantage because of decreased competition with the majority (Box 1).

For asexual populations, the advantage of rarity means that phenotypes on opposite sides of the fitness minimum can coexist in a protected polymorphism 11, 12. Disruptive selection acts to drive the coexisting types further apart, until they reside on different fitness peaks (Box 1, Figure Ic). In freely interbreeding sexual populations, however, the distribution of phenotypes is constrained by the processes of segregation and recombination, which cause many individuals to have the maladaptive intermediate phenotype 13, 14. As a consequence, processes that prevent the production of intermediates are favored, and it is these that we consider here. In addition to competition for resources, other ecological interactions can cause disruptive selection 10, 15. Common types can, for instance, be at a disadvantage by attracting the attention of their predators, experiencing increased incidence of disease, or having too few mutualists.

Empirical support for these theoretical insights is hard to come by owing to substantial experimental difficulties. However, it has recently been demonstrated that intraspecific competition for food in sticklebacks Gasterosteus aculeatus can favor both limnetic and benthic specialist phenotypes over generalists [16]. Other studies have shown that competition produces negative frequency dependence between phenotypes 17, 18, 19, 20.

The twin realizations that disruptive selection can persist for significant periods of time and that many ecological scenarios produce just this sort of selection regime has triggered a massive effort among theoreticians to explore the evolutionary consequences of such scenarios. To date, the consequence that has attracted the most attention is the phenomenon of evolutionary branching of a lineage 15, 21, 22, including the possibility of sympatric speciation 23, 24, 25. However, splitting of a single lineage into genetically distinct lineages is not the only possible response to disruptive selection.

There is presently a limited awareness of the full spectrum of possible adaptive responses to disruptive selection and how to assess their relative likelihoods. All of the potential responses are characterized by a reduction or elimination of disruptive selection via some increase in the diversity of phenotypes and there are many ways in which this can be realized. Although much remains to be learned about the relative frequency of different responses to prolonged disruptive selection, it is unlikely that sympatric speciation will be the most common one. To appreciate the scope of disruptive selection as a creative evolutionary force, it is therefore important to understand the circumstances favoring the different potential responses to this form of natural selection.

Section snippets

Adaptive responses to disruptive selection

Here, we use ‘disruptive selection’ to refer to the second scenario above, where disruptive selection acts to increase phenotypic variation. The possible processes leading to such an increase can be roughly subdivided into three categories, consisting of those that lead to an increase in genetic variation within a species, those that lead to an increase in phenotypic variation without an increase in genetic variation, and those involving other species in the community (Table 1).

Which response should we expect?

As we have illustrated, various processes can be triggered by disruptive selection. To evaluate the importance of disruptive selection for biological evolution, one needs to be aware of this spectrum and of the circumstances favoring one process over the others. Much recent interest in disruptive selection has focused on sympatric speciation. Although an interesting topic, it should be compared with other outcomes that might be more common, given the broad spectrum of possibilities. It is also

Conclusion

Disruptive selection has regained a prominent role in evolutionary thinking, especially in speciation research. The revival of interest in this category of natural selection seems justified, based on the large number of ecological scenarios that could lead to frequency-dependent disruptive selection. We suggest that, to better understand the effects of such selection on biological diversity, future work must develop a more systematic understanding of the full spectrum of responses that can

Acknowledgements

We thank Aneil Agrawal for comments and discussion. C.R. was supported by the Research Council for Earth and Life Sciences with financial aid from the Netherlands Organization of Scientific Research (NWO). P.A.A. and C.R. were supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada. T.V.D. was supported by a Dutch NWO-VENI grant and O.L. thanks the Swedish Research Council for support.

Glossary

Assortative mating:
when sexually reproducing organisms tend to mate with individuals that are similar to themselves in some respect. Can be caused by assortative mate choice, or by environmental factors that cause non-random associations between mating partners.
Attractor:
in dynamical systems, an attractor is a set to which the system approaches given enough time. Trajectories moving close to the attractor remain close when slightly disturbed. Stable equilibrium points, cycles and strange

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