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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 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.
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Phylogenomic analysis of the Lake Kronotskoe species flock of Dolly Varden charr reveals genetic and developmental signatures of sympatric radiation
Recent adaptive radiations provide experimental opportunities to parse the relationship between genomic variation and the origins of distinct phenotypes. Sympatric radiations of the charr complex (genus Salvelinus) present a trove for phylogenetic analyses as charrs have repeatedly diversified into multiple morphs with distinct feeding specializations. However, charr species flocks normally comprise only two to three lineages. Dolly Varden charr inhabiting Lake Kronotskoe represent the most extensive radiation described for the genus, containing at least seven lineages, each with defining morphological and ecological traits. Here, we perform the first genome-wide analysis of this species flock to parse the foundations of adaptive change. Our data support distinct, reproductively isolated lineages within the clade. We find that changes in genes associated with thyroid signaling and craniofacial development provided a foundational shift in evolution to the lake. The thyroid axis is further implicated in subsequent lineage partitioning events. These results delineate a genetic scenario for the diversification of specialized lineages and highlight a common axis of change biasing the generation of specific forms during adaptive radiation.
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- Award ID(s):
- 1845513
- PAR ID:
- 10623861
- Publisher / Repository:
- The Company of Biologists
- Date Published:
- Journal Name:
- Development
- Volume:
- 151
- Issue:
- 20
- ISSN:
- 0950-1991
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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 of 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.more » « less
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Josephs, Emily (Ed.)Abstract Adaptive radiations are characterized by rapid ecological diversification and speciation events, leading to fuzzy species boundaries between ecologically differentiated species. Adaptive radiations are therefore key systems for understanding how species are formed and maintained, including the role of de novo mutations versus preexisting variation in ecological adaptation and the genome-wide consequences of hybridization events. For example, adaptive introgression, where beneficial alleles are transferred between lineages through hybridization, may fuel diversification in adaptive radiations and facilitate adaptation to new environments. In this study, we employed whole-genome resequencing data to investigate the evolutionary origin of hummingbird-pollinated flowers and to characterize genome-wide patterns of phylogenetic discordance and introgression in Penstemon subgenus Dasanthera, a small and diverse adaptive radiation of plants. We found that magenta hummingbird-adapted flowers have apparently evolved twice from ancestral blue-violet bee-pollinated flowers within this radiation. These shifts in flower color are accompanied by a variety of inactivating mutations to a key anthocyanin pathway enzyme, suggesting that independent de novo loss-of-function mutations underlie the parallel evolution of this trait. Although patterns of introgression and phylogenetic discordance were heterogenous across the genome, a strong effect of gene density suggests that, in general, natural selection opposes introgression and maintains genetic differentiation in gene-rich genomic regions. Our results highlight the importance of both de novo mutation and introgression as sources of evolutionary change and indicate a role for de novo mutation in driving parallel evolution in adaptive radiations.more » « less
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Adaptive radiations are bursts in biodiversity that generate new evolutionary lineages and phenotypes. However, because they typically occur over millions of years, it is unclear how their macroevolutionary dynamics vary through time and among groups of organisms. Phyllostomid bats radiated extensively for diverse diets-from insects to vertebrates, fruit, nectar, and blood-and we use their molars as a model system to examine the dynamics of adaptive radiations. Three-dimensional shape analyses of lower molars of Noctilionoidea (Phyllostomidae and close relatives) indicate that different diet groups exhibit distinct morphotypes. Comparative analyses further reveal that phyllostomids are a striking example of a hierarchical radiation; phyllostomids' initial, higher-level diversification involved an "early burst" in molar morphological disparity as lineages invaded new diet-affiliated adaptive zones, followed by subsequent lower-level diversifications within adaptive zones involving less dramatic morphological changes. We posit that strong selective pressures related to initial shifts to derived diets may have freed molars from morpho-functional constraints associated with the ancestral molar morphotype. Then, lineages with derived diets (frugivores and nectarivores) diversified within broad adaptive zones, likely reflecting finer-scale niche partitioning. Importantly, the observed early burst pattern is only evident when examining molar traits that are strongly linked to diet, highlighting the value of ecomorphological traits in comparative studies. Our results support the hypothesis that adaptive radiations are commonly hierarchical and involve different tempos and modes at different phylogenetic levels, with early bursts being more common at higher levels.more » « less
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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, 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.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/dev.203002
