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1. Ecological Diversification in an Adaptive Radiation of Plants: The Role of De Novo Mutation and Introgression

   https://doi.org/10.1093/molbev/msae007  

   Stone, Benjamin W; Wessinger, Carolyn A (January 2024, Molecular Biology and Evolution)

   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. 

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2. Population Genomics of Adaptive Radiation

   https://doi.org/10.1111/mec.17574  

   Combrink, Lucia L; Golcher‐Benavides, Jimena; Lewanski, Alexander L; Rick, Jessica A; Rosenthal, William C; Wagner, Catherine E (December 2024, Molecular Ecology)

   ABSTRACT Adaptive radiations are rich laboratories for exploring, testing, and understanding key theories in evolution and ecology because they offer spectacular displays of speciation and ecological adaptation. Particular challenges to the study of adaptive radiation include high levels of species richness, rapid speciation, and gene flow between species. Over the last decade, high‐throughput sequencing technologies and access to population genomic data have lessened these challenges by enabling the analysis of samples from many individual organisms at whole‐genome scales. Here we review how population genomic data have facilitated our knowledge of adaptive radiation in five key areas: (1) phylogenetics, (2) hybridization, (3) timing and rates of diversification, (4) the genomic basis of trait evolution, and (5) the role of genome structure in divergence. We review current knowledge in each area, highlight outstanding questions, and focus on methods that facilitate detection of complex patterns in the divergence and demography of populations through time. It is clear that population genomic data are revolutionising the ability to reconstruct evolutionary history in rapidly diversifying clades. Additionally, studies are increasingly emphasising the central role of gene flow, re‐use of standing genetic variation during adaptation, and structural genomic elements as facilitators of the speciation process in adaptive radiations. We highlight hybridization—and the hypothesized processes by which it shapes diversification—and questions seeking to bridge the divide between microevolutionary and macroevolutionary processes as rich areas for future study. Overall, access to population genomic data has facilitated an exciting era in adaptive radiation research, with implications for deeper understanding of fundamental evolutionary processes across the tree of life. 

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3. Geographic and Ecological Dimensions of Host Plant-Associated Genetic Differentiation and Speciation in the Rhagoletis cingulata (Diptera: Tephritidae) Sibling Species Group

   https://doi.org/10.3390/insects10090275  

   Doellman, M; Schuler, H; Saintjean, G.; Hood, G.; Egan, S.; Powell, T.; Glover, M; Bruzzese, D.; Smith, J.; Yee, W.; et al (August 2019, Insects)

   Ascertaining the causes of adaptive radiation is central to understanding how new species arise and come to vary with their resources. The ecological theory posits adaptive radiation via divergent natural selection associated with novel resource use; an alternative suggests character displacement following speciation in allopatry and then secondary contact of reproductively isolated but ecologically similar species. Discriminating between hypotheses, therefore, requires the establishment of a key role for ecological diversification in initiating speciation versus a secondary role in facilitating co-existence. Here, we characterize patterns of genetic variation and postzygotic reproductive isolation for tephritid fruit flies in the Rhagoletis cingulata sibling species group to assess the significance of ecology, geography, and non-adaptive processes for their divergence. Our results support the ecological theory: no evidence for intrinsic postzygotic reproductive isolation was found between two populations of allopatric species, while nuclear-encoded microsatellites implied strong ecologically based reproductive isolation among sympatric species infesting different host plants. Analysis of mitochondrial DNA suggested, however, that cytoplasmic-related reproductive isolation may also exist between two geographically isolated populations within R cingulata. Thus, ecology associated with sympatric host shifts and cytoplasmic effects possibly associated with an endosymbiont may be the key initial drivers of the radiation of the R. cingulata group. 

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4. Neotropics as a Cradle for Adaptive Radiations

   https://doi.org/10.1101/cshperspect.a041452  

   Guevara-Andino, Juan E; Dávalos, Liliana M; Zapata, Felipe; Endara, María José; Cotoras, Darko D; Chaves, Jaime; Claramunt, Santiago; López-Delgado, Julia; Mendoza-Henao, Angela M; Salazar-Valenzuela, David; et al (May 2024, Cold Spring Harbor Perspectives in Biology)

   Neotropical ecosystems are renowned for numerous examples of adaptive radiation in both plants and animals resulting in high levels of biodiversity and endemism. However, we still lack a comprehensive review of the abiotic and biotic factors that contribute to these adaptive radiations. To fill this gap, we delve into the geological history of the region, including the role of tectonic events such as the Andean uplift, the formation of the Isthmus of Panama, and the emergence of the Guiana and Brazilian Shields. We also explore the role of ecological opportunities created by the emergence of new habitats, as well as the role of key innovations, such as novel feeding strategies or reproductive mechanisms. We discuss different examples of adaptive radiation, including classic ones like Darwin's finches and Anolis lizards, and more recent ones like bromeliads and lupines. Finally, we propose new examples of adaptive radiations mediated by ecological interactions in their geological context. By doing so, we provide insights into the complex interplay of factors that contributed to the remarkable diversity of life in the Neotropics and highlight the importance of this region in understanding the origins of biodiversity. 

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5. The paradox behind the pattern of rapid adaptive radiation: how can the speciation process sustain itself through an early burst?

   Martin, CH; Richards, EJ (January 2019, Annual review of ecology, evolution, and systematics)

   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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