Abstract
Understanding how and why rates of evolutionary diversification vary is a key issue in evolutionary biology, ecology, and biogeography, and the metaphorical concepts of adaptive radiation and evolutionary stasis describe two opposing aspects causing variation in diversification rates. Here we review the central concepts in the evolutionary diversification literature and synthesize these into a simple, general framework for studying rates of diversification and quantifying their underlying dynamics, which can be applied across clades and regions and across spatial and temporal scales. Our framework describes the diversification rate (d) as a function of the abiotic environment (a), the biotic environment (b) and clade-specific phenotypes or traits (c); thus d∼a,b,c. We refer to the four components (a–d) and their interactions collectively as the ‘Evolutionary Arena’. We outline analytical approaches to this framework and present a case study on conifers, for which we parameterise the general model. We also discuss three conceptual examples: the Lupinus radiation in the Andes in the context of emerging ecological opportunity and fluctuating connectivity due to climatic oscillations; oceanic island radiations in the context of island formation and erosion; and biotically driven radiations of the Mediterranean orchid genus Ophrys. The results of the conifer case study are consistent with the long-standing scenario that low competition and high rates of niche evolution promote diversification. The conceptual examples illustrate how using the synthetic Evolutionary Arena framework helps to identify and structure future directions for research on evolutionary radiations. In this way, the Evolutionary Arena framework promotes a more general understanding of variation in evolutionary rates by making quantitative results comparable between case studies, thereby allowing new syntheses of evolutionary and ecological processes to emerge.
Footnotes
sigrid.liede{at}uni-bayreuth.de, peter.linder{at}systbot.uzh.ch, colin.hughes{at}systbot.uzh.ch, laura.pineiro{at}systbot.uzh.ch, onsteinre{at}gmail.com, matt.larcombe{at}otago.ac.nz, philipp.schlueter{at}uni-hohenheim.de, luis.valente{at}naturalis.nl, carl.beierkuhnlein{at}uni-bayreuth.de., vanessa.cutts{at}nottingham.ac.uk, richard.field{at}nottingham.ac.uk, michael.donoghue{at}yale.edu; erika.edwards{at}yale.edu., s.g.a.flantua{at}gmail.com, steven.higgins{at}uni-bayreuth.de, anke.jentsch{at}uni-bayreuth.de, pirie{at}uni-mainz.de., michael.pirie{at}uib.no
Glossary
- Adaptation
- a trait is an adaptation to a selective regime if it evolved in response to selection by that regime (Gould & Vrba, 1982)
- Adaptive zone
- a fitness peak in a set of related niches (the adaptive grid or macroevolutionary landscape) that a lineage occupies by virtue of a novel trait(s) that confer fitness in these niches.
- Confluence
- the sequential coming together of a set of traits (innovations and synnovations), environmental changes, and geographic movements along the branches of a phylogenetic tree (Donoghue & Sanderson, 2015).
- Disparification
- increase in trait variance in a clade through time. That is, increase in measurable phenotypic differences among taxa, whereas the traits in question may be morphological, anatomical, physiological, genetic, behavioural, etc. Disparification is a characteristic of adaptive radiation.
- Diversification
- increase in the taxonomic diversity in a clade through time. The diversification rate is defined as speciation minus extinction and can thus be negative.
- Ecological opportunity
- lineage-specific environmental conditions that contain both niche availability and niche discordance, favouring adaptation and promoting diversifying selection within the lineage (adapted from Wellborn & Langerhans, 2015).
- Exaptation
- a trait that has evolved for one use, and that is later useful for another usage (sometimes deceptively termed ‘pre-adaptation’; adapted from de Vladar et al., 2017). The original definition of Gould and Vrba (1982) is: “features that now enhance fitness but were not built by natural selection for their current role”.
- Extrinsic factor
- environmental factors such as abiotic and biotic niche parameters, not inherited genetically by the focal lineage.
- Intrinsic factor
- phenotypic (morphological, physiological) or genetic trait(s), inherited by the focal lineage.
- Key event
- events that trigger a shift in diversification rates.
- Key innovation
- new trait which facilitates the occupation of a new adaptive zone, or which breaks an evolutionary constraint; i.e. “phenotypes that allowed a species to interact with the environment in a novel way” (Stroud & Losos, 2016, p 508).
- Phenotype
- a set of features of an individual that stems from the interactions between genotype and environment.
- Radiation
- accelerated proliferation of species and/or phenotypes, in the sense of significant increase in the diversification and/or disparification rate compared to background rates (without a shift/ significant rate increase, it is not a radiation but [background] diversification / disparification). Radiation (diversification / disparification) can be combined with an epithet, such as adaptive, geographical, ecological, or genetical (gene flow) to further describe the nature of the evolutionary forces and situations (e.g., ‘sexual radiation’ may refer to radiation driven by sexual selection, or ‘montane radiation’ to radiation in mountains, ‘insular radiation’ to radiations on islands, or simply ‘cichlid radiation’ to refer to a certain lineage, etc.). We refer to biological radiation most generally as ‘evolutionary radiation’ as the change in diversification / disparification rates has macro-evolutionary consequences. In addition, there are two prominent concepts that refer to the process underlying the evolutionary radiations:
- Adaptive radiation
- proliferation of species driven by the evolution of phenotypic (ecological and/or morphological) diversity that can be linked to adaptation to an environment. The environment may act as a modulator, driving (potentially sympatric) speciation and/or slowing extinction.
- Geographic radiation
- proliferation of species driven by enhanced opportunities for allopatric speciation (reproductive isolation resulting from spatial barriers) in a particular region (modified from Simões et al., 2016). Also referred to as ‘non-adaptive radiation’ (= geographic), or ‘climatic radiation’ when differing climates are thought important. Note that the adaptive and geographic categories are simplified: both adaptive and neutral processes likely play a role in modulating diversification rates in most radiations, but their relative contributions differ. For example, ecological factors may enhance the opportunity for reproductive isolation, and species divergence in adaptive radiations may additionally be promoted by spatial isolation (see main text, Drivers of evolutionary radiations).
- Synnovation
- interacting combination of traits with a particular consequence (Donoghue & Sanderson, 2015).
- Trait
- a heritable attribute of evolutionary lineages (genes, individuals, populations, species, clades) that can be observed.
- Trigger
- Event or situation starting a radiation.
