Opinion
The Ecology of Nonecological Speciation and Nonadaptive Radiations

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Highlights

Nonadaptive radiations result from nonecological speciation and the absence of character displacement.

There are properties of organisms and ecosystems that make nonadaptive radiations more or less likely.

As our understanding of cryptic species increases, we are likely to become aware of more nonadaptive radiations.

Nonadaptive radiations can give rise to functional redundancy in ecosystems, which is likely to be correlated with resilience and/or resistance to perturbation.

Understanding the ecology of why competitive exclusion is mitigated is essential for the conservation of biodiversity.

Growing evidence for lineage diversification that occurs without strong ecological divergence (i.e., nonadaptive radiation) challenges assumptions about the buildup and maintenance of species in evolutionary radiations, particularly when ecologically similar and thus potentially competing species co-occur. Understanding nonadaptive radiations involves identifying conditions conducive to both the nonecological generation of species and the maintenance of co-occurring ecologically similar species. To borrow MacArthur’s [1] (Challenging Biological Problems 1972;253–259) form of inquiry, the ecology of nonadaptive radiations can be understood as follows: for species of type A, in environments of type B, nonadaptive radiations may emerge. We review purported cases of nonadaptive radiation and suggest properties of organisms, resources, and landscapes that might be conducive to their origin and maintenance. These properties include poor dispersal ability and the ephemerality and patchiness of resources.

Section snippets

On the Origin of Nonadaptive Radiations

Thirteen years after the publication of On the Origin of Species by Means of Natural Selection, Gulick [2] suggested that the most species-rich groups of land snails in Hawaii might have diversified for reasons having little to do with natural selection (see Glossary). Although these species were distinguishable by shell characters, their shells seemed unlikely to be correlated with adaptations to different environments: ‘The conditions under which they live are so completely similar, that it

Properties of Organisms

Since nonadaptive radiations involve both elevated diversification and lack of clade-wide disparity in resource usage, identifying the properties of organisms connected with these factors should help us both uncover and understand nonadaptive radiations. Diversification and lack of disparity may often have different mechanistic underpinnings, so it is useful to consider them separately (Table 2). Understanding which species are prone to geographic isolation and thus allopatric speciation is of

Geography of Nonadaptive Radiation

Geographic distribution is important for understanding species’ evolution and ecology but its interpretation with respect to diversification mode is not always straightforward. Many presently sympatric species are likely to have speciated in allopatry at some point prior. The underlying process at the time of speciation, millions of years ago in some cases, can be difficult to uncover [52], which complicates our understanding of both adaptive and nonadaptive radiations. Many currently sympatric

Community Ecology of Avoiding Competitive Exclusion

In this Opinion article, we treat competition for resources as the primary factor that usually prevents geographic range overlap between ecologically similar taxa. Competitive exclusion is most convincingly demonstrated in small areas (e.g., Petri dishes [64]), but many taxa exist in metapopulations where local extirpation can be balanced by dispersal 67, 68. Patchily distributed, ephemeral resources are permissive of a variety of processes that can allow high degrees of niche overlap at

Concluding Remarks: Macroecology and Conservation Biology of Nonadaptive Radiations

If there is a large-scale geographic gradient of one of the properties of resources and/or habitats that is conducive to nonadaptive radiations, one might expect nonadaptive radiations to be more likely in some places than in others. Chase [91] showed that stochastic assembly is more important in more productive environments (as measured by available phosphorus). This could lead to a positive relationship between species richness and productivity at regional scales that include many smaller

Acknowledgments

We thank Erik Svensson and five anonymous reviewers for their thoughtful and thought-provoking criticisms and comments, which improved this Opinion article. J.E.C-M. thanks Jack Stanford, Mike Kaspari, David Hambright, Adam Kay, Ola Fincke, Brad Stevenson, Bob Nairn, Natalie Clay, Carla Atkinson, David Donoso, Rich Zamor, Jessica Beyer, Thayer Hallidayschult, and Kim Myers for their important discussions on ecology. Both authors thank Warren Allmon for permission to use the framework that

Glossary

Adaptive radiation
(i) a pattern of species diversification in which a lineage of species occupies a diversity of ecological roles [90]; and (ii) the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage 7, 15, 19.
Beta diversity
can be thought of as the difference between assemblages; in the context of patchy habitats it is sometimes formally defined as the ratio of gamma (regional, or landscape level) diversity to average alpha (local, or patch level) diversity.

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