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PLOS Biology: New Articles

  • Ancient inversion polymorphisms associate with sexually selected traits across natural guppy populations

    by Yuying Lin, Wouter van der Bijl, Judith E. Mank

    Understanding the distribution, frequency, and long-term persistence of chromosomal inversions in natural populations is key to understanding population evolution and adaptive processes. Inversions often span multiple genes, are subject to strong selective pressures and can affect complex traits. Here, we used an unbiased method to identify inversions in guppies from three different Trinidadian rivers with paired high- and low-predation populations which differ in a wide range of morphological, behavioural and life-history traits. We identified 22 inversions, ranging in age from 1 to 6 million years, which are widespread across the genome and predate the colonisation of each river. We were able to verify the breakpoints for all but one of these inversions using linked reads. We find three inversions that are significantly associated with local adaptation syndromes in high- versus low-predation populations, however, none are reciprocally fixed throughout all three replicate rivers. Additionally, we observe seven additional inversions maintained in all three rivers without evidence of local adaptation. Simulations reveal that the level of inversion polymorphism that we observe is far greater than expected under a neutral model. We observed a significant overlap between polymorphic inversions and loci previously implicated in male ornament pattern variation in guppies, suggesting that negative frequency-dependent selection due to female preference for male pattern novelty might explain the maintenance of inversion polymorphism. Overall, our results show the role of sexual selection in the long-term maintenance of inversion polymorphisms, and an interplay between sexual and natural selection in frequency dynamics.

  • Coordinated P450–UGT detoxification contributes to furanocoumarin tolerance associated with host plant range divergence in <i>Helicoverpa</i>

    by Huidong Wang, Yajie Kong, Xinyue Su, Yu Shi, Jianpeng Zhang, Yinjia Wang, Yajuan Xiao, Xing Geng, Jing Song, Yueru Ye, Kairan Zuo, Chris Bass, Shutang Zhou

    Plants and herbivorous insects are engaged in a continuous evolutionary arms race driven by chemical defences and counter-defences. How insects integrate distinct detoxification systems to overcome diverse phytochemicals, and how such mechanisms contribute to host-range divergence, remains poorly understood. Here, we uncover a cooperative cytochrome P450–UDP-glycosyltransferase (UGT) cascade that mediates furanocoumarin tolerance in Helicoverpa armigera. Comparative genomic analyses across Helicoverpa and related noctuid species revealed that the UGT33 family is the most extensively expanded and dynamically diversified UGT lineage in Helicoverpa. Targeted CRISPR–Cas9 knockouts of UGT33 gene clusters in polyphagous H. armigera demonstrated their essential roles in detoxifying the furanocoumarins xanthotoxin and imperatorin. Combined metabolic and functional assays further established a sequential detoxification pathway, in which the cytochrome P450 CYP6AE19 catalyses either the O-dealkylation of xanthotoxin to yield xanthotoxol or the aromatic-carbon hydroxylation of xanthotoxin to form 5-hydroxyxanthotoxin, which are subsequently glycosylated by UGT33 enzymes to form their less-toxic glucosides. In contrast, impaired CYP6AE19–UGT33 coordination in the oligophagous Helicoverpa assulta was associated with reduced xanthotoxin detoxification and high sensitivity to this compound. Together, these findings provide direct evidence for coordinated Phase I–Phase II detoxification of a plant defensive compound in insects and show that functional divergence in this pathway contributes to interspecific differences in plant toxin tolerance, which are associated with contrasting dietary breadth in closely related herbivorous insects.

  • Pathogen subversion of neuro-epidermal signaling impairs lysosomal function to disrupt collagen homeostasis in <i>Caenorhabditis elegans</i>

    by Qian Li, Yating Liu, Hanyi Chen, Weilie Xiao, Bin Qi

    The epidermis relies on collagen-rich extracellular matrices (ECMs) to maintain barrier integrity against pathogens. Lysosomes regulate cuticle collagen turnover, yet how neuronal signaling modulates epidermal lysosomal function and collagen organization during infection remains unclear. Using Pseudomonas aeruginosa PA14-Caenorhabditis elegans infection model, we demonstrate that pathogen-induced neuronal signaling disrupts epidermal lysosomal activity and collagen remodeling. PA14 infection triggers neurons to secrete NSIF-1 (Neuronal Secreted Immune Factor 1), which translocates to the epidermis and impairs lysosomal acidification, maturation, and degradation by suppressing the transcription factor ELT-3. This disruption leads to disorganized collagen structure, compromising cuticle integrity and host resistance. Genetic mutation of nsif-1 restores lysosomal function, enhances collagen density, and improves survival, while neuron-specific nsif-1 knockdown confirms its neuronal origin. Moreover, NSIF-1 inhibits ELT-3 nuclear localization, blocking its role in lysosomal-dependent ECM repair. Our study reveals a neuro-epidermal axis wherein pathogens exploit neuronal signals to disrupt lysosomal function and collagen homeostasis, identifying NSIF-1 and ELT-3 as potential targets to counteract infection-driven ECM dysregulation.

  • Antibodies targeting phage fiber and nozzle proteins impair <i>Acinetobacter baumannii</i> phage therapy by blocking infection and promoting immune clearance

    by Heng Xue, Xinfeng Li, Guibo Rao, Fen Hu, Mingyue Zhong, Paulina Miernikiewicz, Rui Qiu, Sheng Cao, Krystyna Dąbrowska, Hang Yang

    Phage therapy represents a promising strategy to tackle the growing threat of antimicrobial resistance. Increasing evidence has demonstrated that phage-specific antibodies may compromise the efficacy of phage therapy. Nevertheless, little is known about how phage protein specificity of antibodies modulates phage therapeutic outcomes. Herein, we utilized AbP20, a podovirus against Acinetobacter baumannii, to explore the effects of antibodies elicited by each structural protein on phage therapy efficacy in a mouse infection model. Intraperitoneal administration of AbP20 once a day for 7 consecutive days induced robust phage-specific antibody responses that impaired phage therapy. Genome-guided antigen screening identified that antibodies elicited by the nozzle and fiber proteins of AbP20, rather than those targeting the portal, capsid, or adaptor proteins, are the dominant drivers of phage therapy failure. Specifically, fiber-specific and nozzle-specific antibodies block bacterial adsorption and genomic injection of AbP20, respectively. Meanwhile, both antibody subsets efficiently induce large phage aggregates and potentiate macrophage phagocytosis via an Fc receptor-independent pathway. An evolved AbP20 variant with improved neutralization escape capacity exhibited comparable antibody-accelerated phagocytosis and host immune clearance, yet partially rescued therapeutic failure caused by neutralizing antibodies. Collectively, this study elucidates that nozzle- and fiber-elicited neutralizing antibodies impair phage therapy via dual synergistic mechanisms, which offers novel insights into the multifaceted modulation of phage-specific antibodies against phage therapeutic efficacy.

  • Who Eats Whom? A global food web derived from citizen science

    by Bradley C. Allf, Aditi Mallavarapu, David W. Kikuchi, Nikhil Vasudeva, Robert R. Dunn

    Citizen science contains abundant yet underutilized data about species interactions. We present Who Eats Whom, a database and public engagement tool for searching and visualizing thousands of feeding relationships derived from iNaturalist data. Citizen science photographs contain a vast and underused record of species interactions. This Community Page introduces Who Eats Whom, an interactive, searchable food web created from photographs uploaded to iNaturalist.