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.
Keywords
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Glossary
Adaptive radiation
(i) a pattern of species diversification in which a lineage of species occupies a diversity of ecological roles [
Beta diversity
90
]; and (ii) the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage [
7
,
15
,
19
].
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. If a set, small number of species can occupy small habitat patches, increasing beta diversity among patches will necessarily increase gamma diversity.
Coexistence
Siepielski and McPeek [
Community assembly
58
] make the distinction between co-occurrence and coexistence of species, the latter of which implies some level of population stability among community members at the local scale that is stabilized by species traits and niches. This is in contrast to co-occurrence, where species’ presence in a community is largely due to chance or larger-scale processes.
the construction and maintenance of local communities through sequential, repeated immigration of species from the regional species pool. Vellend [
Co-occurrence
68
] usefully suggests that species membership in assemblages at various scales is driven by the processes of speciation, extirpation, migration, and ecological drift.
refers to species that are found together by chance or because of larger-scale processes, like source–sink dynamics. Neutral species co-occur.
Disparification
increase in the morphospace occupied by members of a clade through time [
Diversification
102
,
103
]; distinct from diversification, which we use here to mean an increase in the number of species in a clade through time. Nonadaptive radiations are expected to exhibit diversification with minimal disparification.
net increase in the number of species in a clade over time. Speciation minus extinction.
Ecological drift
random fluctuation in species abundances in an assemblage, analogous to genetic drift of allele frequency in a population (see [
Ecological speciation
68
]).
the generation of reproductive isolation between populations as a result of ecologically based divergent selection between environments, which can include both natural and sexual selection [
,
].
Janzen–Connell–Thingstad dynamics
a family of negative density-dependent selection (NDDS) or negative frequency-dependent selection (NFDS) processes that are very similar, although Janzen–Connell is typically invoked by tropical forest biologists, whereas Thingstad’s ‘Kill-the-Winner’ hypothesis is much more frequently cited in the marine phage literature [
Natural selection
86
,
87
].
differential survival and/or reproduction of classes of entities (alleles, genotypes, subsets of genotypes, populations, species) that differ in one or more characteristics.
Negative density-dependent selection (NDDS)
sometimes referred to as ‘inverse’ density-dependent selection; selection that favors rare phenotypes. Although technically distinct, NFDS has similar effects on community-level dynamics, as frequency is often related to density. One way that NDDS and NFDS dynamics can arise is through species-specific pathogens, which will tend to lead to some variation of Janzen–Connell–Thingstad dynamics. Another possible way that NDDS or NFDS can occur is through sexual conflict [
Neutral species
61
,
- Kobayashi K.
Sexual selection sustains biodiversity via producing negative density-dependent population growth.
J. Ecol. 2018; (Published online November 13, 2018)https://doi.org/10.1111/1365-2745.13088
104
]. Throughout this Opinion article, we refer to population dynamics among (not within) species; that is, our discussion focuses on species richness rather than intraspecific genetic diversity.
species that are ecologically nearly identical to one another and that follow the neutral dynamics of a random walk in relative frequency as described by Hubbell [
Niche
105
]; one of the four types of species in a community identified by McPeek [
69
] based on their population dynamical properties.
the environmental conditions that allow a species to satisfy its minimum requirements so that the birth rate of a local population is equal to or greater than its death rate, along with the set of per capita effects of that species on these environmental conditions [
Niche conservatism
70
,
106
].
a pattern where closely related species are more ecologically similar to one another than would be expected based on their phylogenetic relationships. Niche conservatism is not expected in an adaptive radiation.
Nonadaptive radiation
lineage diversification with minimal ecological diversification, often (but not always) resulting in allopatric or parapatric taxa. ‘Minimal’ refers to slight differences among species that can accumulate in allopatry; for example, due to neutral evolution or slight differences in environments [
Nonecological speciation
24
] (Box 1).
the generation of reproductive isolation between populations that does not arise from divergent natural selection [
]. One potential mechanism by which nonecological speciation can occur involves the slow process of fixation of different and selectively favored mutations among allopatric populations.
Priority effects
a pattern whereby the outcome of competition for a resource is highly influenced by the (often stochastic) order of arrival. For example, some types of wood-rot fungi will be able to exclude competitors only if they are established first [
Probability refuge
70
,
80
]. A related mathematical model of stochastic community assembly is the ‘Lottery Hypothesis’ [
78
,
107
].
a metaphorical ‘refuge’ concept that Shorrocks and others [
Sexual selection
60
,
71
,
72
,
75
] invoke in the aggregation model to describe the niche space that opens for ecologically similar species when intraspecific competition is stronger than interspecific competition (e.g., due to aggregated egg laying and sibling competition in ephemeral patchy resources).
selection on traits resulting from differential mating success, including access to different numbers of mates or to mates of differing quality [
] (Box 3).
Sink species
species that are present only due to continual migration from other communities; one of the four types of species in a community identified by McPeek [
Source–sink dynamics
69
] based on its population dynamical properties.
movement of individuals between high-quality (source) and lower-quality (sink) patches within a metacommunity, where populations in the sink are sustained only through migration.
Walking-dead species
species that are slowly being driven extinct by the ecological conditions that they experience within the community − immigration will not rescue them; one of the four types of species in a community identified by McPeek [
69
] based on its population dynamical properties.
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Published online: February 26, 2019
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