skip to main content

Title: The paradox behind the pattern of rapid adaptive radiation: how can the speciation process sustain itself through an early burst?
Rapid adaptive radiation poses a distinct question apart from speciation and adaptation: what happens after one speciation event? That is, how are some lineages able to continue speciating through a rapid burst? This question connects global macroevolutionary patterns to microevolutionary processes. Here we review major features of rapid radiations in nature and their mismatch with theoretical models and what is currently known about speciation mechanisms. Rapid radiations occur on three major diversification axes – species richness, phenotypic disparity, and ecological diversity – with exceptional outliers on each axis. The paradox is that the hallmark early stage of adaptive radiation, a rapid burst of speciation and niche diversification, is contradicted by most existing speciation models which instead predict continuously decelerating speciation rates and niche subdivision through time. Furthermore, while speciation mechanisms such as magic traits, phenotype matching, and physical linkage of co-adapted alleles promote speciation, it is often not discussed how these mechanisms could promote multiple speciation events in rapid succession. Additional mechanisms beyond ecological opportunity are needed to understand how rapid radiations occur. We review the evidence for five emerging theories: 1) the ‘transporter’ hypothesis: introgression and the ancient origins of adaptive alleles, 2) the ‘signal complexity’ hypothesis: the dimensionality more » of sexual traits, 3) the connectivity of fitness landscapes, 4) ‘diversity begets diversity’, and 5) flexible stem/‘plasticity first’. We propose new questions and predictions to guide future work on the mechanisms underlying the rare origins of rapid radiation. « less
Award ID(s):
Publication Date:
Journal Name:
Annual review of ecology, evolution, and systematics
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Adaptive radiations are characterized by the rapid proliferation of species. Explaining how adaptive radiations occur therefore depends, in part, on identifying how populations become reproductively isolated––and ultimately become different species. Such reproductive isolation could arise when populations adapting to novel niches experience selection to avoid interbreeding and, consequently, evolve mating traits that minimize such hybridization via the process of reinforcement. Here, we highlight that a downstream consequence of reinforcement is divergence of conspecific populations, and this further divergence can instigate species proliferation. Moreover, we evaluate when reinforcement will––and will not––promote species proliferation. Finally, we discuss empirical approaches to testmore »what role, if any, reinforcement plays in species proliferation and, consequently, in adaptive radiation. To date, reinforcement’s downstream effects on species proliferation remain largely unknown and speculative. Because the ecological and evolutionary contexts in which adaptive radiations occur are conducive to reinforcement and its downstream consequences, adaptive radiations provide an ideal framework in which to evaluate reinforcement’s role in diversification.

    « less
  2. The role of the environmental niche in fostering ecological divergence during adaptive radiation remains enigmatic. In this study, we examine the interplay between environmental niche divergence and conservatism in the context of adaptive radiation on oceanic islands, by characterizing the niche breadth of four Hawaiian arthropod radiations: Tetragnatha spiders (Tetragnathidae Latreille, 1804), Laupala crickets (Gryllidae Otte, 1994), a clade of Drosophila flies (Drosophilidae Fallén, 1823) and Nesosydne planthoppers (Delphacidae Kirkaldy, 1907). We assembled occurrence datasets for the four lineages, modelled their distributions and quantified niche overlap. All four groups occupy the islands in distinct ways, highlighting the contrasting axes ofmore »diversification for different lineages. Laupala and Nesosydne have opposite environmental niche extents (broad and narrow, respectively), whereas Tetragnatha and Drosophila share relatively intermediate tolerances. Temperature constrains the distributions of all four radiations. Tests of phylogenetic signal suggest that, for Tetragnatha and Drosophila, closely related species exhibit similar environmental niches; thus, diversification is associated with niche conservatism. Sister species comparisons also show that populations often retain similar environmental tolerances, although exceptions do occur. Results imply that diversification does not occur through ecological speciation; instead, adaptive radiation occurs largely within a single environment.« less
  3. Abstract Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies,more »ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life.« less
  4. Some lineages radiate spectacularly when colonizing a region, but others do not. Large radiations are often attributed to species’ adaptation into niches, or to other drivers, such as biogeography including dispersal ability and spatial structure of the landscape. Here we aim to disentangle the factors determining radiation size, by modeling simplified scenarios without the complexity of explicit niches. We build a spatially structured neutral model free from niches and incorporating a form of protracted speciation that accounts for gene flow between populations. We find that a wide range of radiation sizes are possible in this model depending on the combinationmore »of geographic isolation and species’ dispersal ability. At extremely low rates of dispersal between patches, each patch maintains its own endemic species. Intermediate dispersal rates foster larger radiations as they allow occasional movement between patches whilst sufficiently restricting gene flow to support further speciation in allopatry. As dispersal rates increase further, a critical point is reached at which demographically identical lineages may vary greatly in radiation size due to rare and stochastic dispersal events. At the critical point in dispersal frequency, some lineages remain a single species for a comparatively long time, whilst others with identical characteristics produce the largest radiations of all via a new mechanism for rapid radiation that we term a ‘radiation cascade’. Given a single species covering many patches connected with gene flow, a radiation cascade is triggered when stochastic dispersal is unusually low for a period, leading to an initial speciation event. This speciation means there are fewer individuals per species and thus further reduced gene flow between conspecifics. Reduced gene flow in turn makes it easier for further speciation to occur. During a radiation cascade, dispersal of individuals between patches continues at the same rate as before, but due to the increasing diversity it primarily introduces novel species that will later speciate, rather than adding to gene flow of existing species. Once a radiation cascade begins, it continues rapidly until it is arrested by a new equilibrium between speciation and extinction. We speculate that such radiation cascades may occur more generally and are not only present in neutral models. This process may help to explain rapid radiation, and the extreme radiation sizes of certain lineages with dispersing ancestors. Whilst niches no doubt play a role in community assembly, our findings lead us to question whether diversification and adaptation into niches is sometimes an effect of speciation and rapid radiation, rather than its cause.« less
  5. To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of adaptive alleles underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. On a single Bahamian island, ancient standing variation from disjunct geographic sources was reassembled into new combinations under strong directional selection for adaptation to the novel trophic niches of scale-eating and molluscivory. We found evidence for two longstanding hypotheses of adaptive radiation: hybrid swarm origins and temporal stages of adaptation. Using a combination of population genomics, transcriptomics, and genome-wide association mapping, we demonstrate that this microendemic adaptivemore »radiation of novel trophic specialists on San Salvador Island, Bahamas experienced twice as much adaptive introgression as generalist populations on neighboring islands and that adaptive divergence occurred in stages. First, standing regulatory variation in genes associated with feeding behavior (prlh,cfap20, andrmi1) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (itga5,ext1,cyp26b1, andgalr2) and finally the only de novo nonsynonymous substitution in an osteogenic transcription factor and oncogene (twist1) swept to fixation most recently. Our results demonstrate how ancient alleles maintained in distinct environmental refugia can be assembled into new adaptive combinations and provide a framework for reconstructing the spatiotemporal landscape of adaptation and speciation.

    « less