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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. Why do hybrids turn down sex?

   https://doi.org/10.1093/evolut/qpad129  

   Fyon, Frédéric; Berbel-Filho, Waldir Miron; Schlupp, Ingo; Wild, Geoff; Úbeda, Francisco; Orive, ed., Maria E.; Chapman, ed., Tracey (July 2023, Evolution)

   Abstract Asexual reproduction is ancestral in prokaryotes; the switch to sexuality in eukaryotes is one of the major transitions in the history of life. The study of the maintenance of sex in eukaryotes has raised considerable interest for decades and is still one of evolutionary biology’s most prominent question. The observation that many asexual species are of hybrid origin has led some to propose that asexuality in hybrids results from sexual processes being disturbed because of incompatibilities between the two parental species’ genomes. However, in some cases, failure to produce asexual F1s in the lab may indicate that this mechanism is not the only road to asexuality in hybrid species. Here, we present a mathematical model and propose an alternative, adaptive route for the evolution of asexuality from previously sexual hybrids. Under some reproductive alterations, we show that asexuality can evolve to rescue hybrids’ reproduction. Importantly, we highlight that when incompatibilities only affect the fusion of sperm and egg’s genomes, the two traits that characterize asexuality, namely unreduced meiosis and the initiation of embryogenesis without the incorporation of the sperm’s pronucleus, can evolve separately, greatly facilitating the overall evolutionary route. Taken together, our results provide an alternative, potentially complementary explanation for the link between asexuality and hybridization. 

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4. Introgression among North American wild grapes (Vitis) fuels biotic and abiotic adaptation

   https://doi.org/10.1186/s13059-021-02467-z  

   Morales-Cruz, Abraham; Aguirre-Liguori, Jonas A.; Zhou, Yongfeng; Minio, Andrea; Riaz, Summaira; Walker, Andrew M.; Cantu, Dario; Gaut, Brandon S. (December 2021, Genome Biology)

   Abstract Background Introgressive hybridization can reassort genetic variants into beneficial combinations, permitting adaptation to new ecological niches. To evaluate evolutionary patterns and dynamics that contribute to introgression, we investigate six wild Vitis species that are native to the Southwestern United States and useful for breeding grapevine ( V. vinifera ) rootstocks. Results By creating a reference genome assembly from one wild species, V. arizonica , and by resequencing 130 accessions, we focus on identifying putatively introgressed regions (pIRs) between species. We find six species pairs with signals of introgression between them, comprising up to ~ 8% of the extant genome for some pairs. The pIRs tend to be gene poor, located in regions of high recombination and enriched for genes implicated in disease resistance functions. To assess potential pIR function, we explore SNP associations to bioclimatic variables and to bacterial levels after infection with the causative agent of Pierce’s disease ( Xylella fastidiosa ). pIRs are enriched for SNPs associated with both climate and bacterial levels, suggesting that introgression is driven by adaptation to biotic and abiotic stressors. Conclusions Altogether, this study yields insights into the genomic extent of introgression, potential pressures that shape adaptive introgression, and the evolutionary history of economically important wild relatives of a critical crop. 

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5. Transgressive hybrids as hopeful holobionts

   https://doi.org/10.1186/s40168-024-01994-8  

   Camper, Benjamin Thomas; Kanes, Andrew Stephen; Laughlin, Zachary Tyler; Manuel, Riley Tate; Bewick, Sharon Anne (January 2025, Microbiome)

   Abstract BackgroundHybridization between evolutionary lineages has profound impacts on the fitness and ecology of hybrid progeny. In extreme cases, the effects of hybridization can transcend ecological timescales by introducing trait novelty upon which evolution can act. Indeed, hybridization can even have macroevolutionary consequences, for example, as a driver of adaptive radiations and evolutionary innovations. Accordingly, hybridization is now recognized as a motor for macrobial evolution. By contrast, there has been substantially less progress made towards understanding the positive eco-evolutionary consequences of hybridization on holobionts. Rather, the emerging paradigm in holobiont literature is that hybridization disrupts symbiosis between a host lineage and its microbiome, leaving hybrids at a fitness deficit. These conclusions, however, have been drawn based on results from predominantly low-fitness hybrid organisms. Studying “dead-end” hybrids all but guarantees finding that hybridization is detrimental. This is the pitfall that Dobzhansky fell into over 80 years ago when he used hybrid sterility and inviability to conclude that hybridization hinders evolution. Goldschmidt, however, argued that rare saltational successes—so-called hopeful monsters—disproportionately drive positive evolutionary outcomes. Goldschmidt’s view is now becoming a widely accepted explanation for the prevalence of historical hybridization in extant macrobial lineages. Aligning holobiont research with this broader evolutionary perspective requires recognizing the importance of similar patterns in host–microbiome systems. That is, rare and successful “hopeful holobionts” (i.e., hopeful monsters at the holobiont scale) might be disproportionately responsible for holobiont evolution. If true, then it is these successful systems that we should be studying to assess impacts of hybridization on the macroevolutionary trajectories of host–microbiome symbioses. ResultsIn this paper, we explore the effects of hybridization on the gut (cloacal) and skin microbiota in an ecologically successful hybrid lizard,Aspidoscelis neomexicanus. Specifically, we test the hypothesis that hybrid lizards have host-associated (HA) microbiota traits strongly differentiated from their progenitor species. Across numerous hybrid microbiota phenotypes, we find widespread evidence of transgressive segregation. Further, microbiota restructuring broadly correlates with niche restructuring during hybridization. This suggests a relationship between HA microbiota traits and ecological success. ConclusionTransgressive segregation of HA microbiota traits is not only limited to hybrids at a fitness deficit but also occurs in ecologically successful hybrids. This suggests that hybridization may be a mechanism for generating novel and potentially beneficial holobiont phenotypes. Supporting such a conclusion, the correlations that we find between hybrid microbiota and the hybrid niche indicate that hybridization might change host microbiota in ways that promote a shift or an expansion in host niche space. If true, hybrid microbiota restructuring may underly ecological release from progenitors. This, in turn, could drive evolutionary diversification. Using our system as an example, we elaborate on the evolutionary implications of host hybridization within the context of holobiont theory and then outline the next steps for understanding the role of hybridization in holobiont research. 

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