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Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation

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Radiations of ecologically and morphologically differentiated sympatric species can exhibit the pattern of a burst of diversification, which might be produced by ecological divergence between populations, together with the acquisition of reproductive isolation (‘ecological speciation’). Here we suggest that this pattern could also arise if speciation precedes significant ecological differentiation (i.e. through geographical isolation and nonadaptive radiation). Subsequently, species ecologically differentiate and spread into sympatry. Alternative routes to producing ecologically differentiated sympatric species are difficult to detect in old radiations. However, nonadaptive radiations are common and might therefore regularly be responsible for currently ecologically differentiated sympatric species (e.g. among groups that are not susceptible to ecological speciation). Species evolving nonadaptively over long periods might eventually replace young, ecologically produced species.

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Contributions of ecological and nonecological speciation to young and old radiations

Adaptive radiations are generally recognized as a pattern of ecological differentiation among a group of related, sympatric, species 1, 2 (see Glossary). Classic contemporary radiations, such as Darwin's finches in the Galápagos [3], or Anolis lizards of the Caribbean [4], contain species that are differentiated in body size and microhabitat, with up to 10 (Darwin's finches) or 11 (Anolis) species being found in some localities. Routes to adaptive radiation lie along a continuum where, at one

Nonadaptive radiations

Gittenberger [10] described nonadaptive radiation as ‘evolutionary diversification from a single ancestor, not accompanied by relevant niche differentiation.’ Here, we define ‘relevant’ as ecological differences that are associated with coexistence in sympatry. Thus, we define a nonadaptive radiation as a collection of related ecologically similar species that are allopatric or parapatric replacements of one another (‘allospecies’ [11]). Such groups of species are common (e.g. in birds [7],

Adaptive radiation and ecological speciation; nonadaptive radiation and nonecological speciation

Ecological speciation is defined as ‘the process by which barriers to gene flow evolve between populations as a result of ecologically based divergent selection’ 5, 6. Divergent sexual or natural selection on one trait, and/or multifarious, divergent selection pressures on multiple traits can generate reproductive isolation as a correlated response 29, 30. Ecological speciation can be rapid, occurring on the order of thousands of years [31], and has been identified in young adaptive radiations

Adaptive differentiation following nonecological speciation

Ecological opportunity might also lead to rapid ecological differentiation after nonecological speciation has occurred. Consider a series of allospecies (Figure 3) and imagine environments change such that multiple niches become available. These species might then spread into each other's range, accompanied by ecological character displacement (i.e. divergence to occupy different parts of niche space; Figure 3d). Because allospecies are already reproductively isolated, they appear to be prime

Conclusion

Given the prominence that has recently been given to the role of ecology in the process of speciation 5, 6, 29, 31, it is important to ask how commonly speciation precedes significant ecological differentiation. This should be generally testable as we gain more knowledge about the history of the Earth. The timing of lineage-splitting events (associated with barrier formation among populations) might be distinguishable from the timing of ecological opportunity (e.g. climate change), promoting

Acknowledgements

We thank R. Gillespie, B. Holland and M. Hadfield for information on their study organisms and for photos, D. Wake for granting figure permission, and D. Liittschwager and S. Middleton for granting permission to use additional spider photos. We thank J. Losos, D. Schluter, J. Weir and two anonymous reviewers for criticism of earlier drafts.

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