Lana Khaldy, Orit Peleg, Claudia Tocco, L Mahadevan, Marcus Byrne, Marie Dacke
{"title":"Correction: The effect of step size on straight-line orientation.","authors":"Lana Khaldy, Orit Peleg, Claudia Tocco, L Mahadevan, Marcus Byrne, Marie Dacke","doi":"10.1098/rsif.2024.0580","DOIUrl":"10.1098/rsif.2024.0580","url":null,"abstract":"","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"21 219","pages":"20240580"},"PeriodicalIF":3.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11522986/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142546200","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Praneet Prakash, Xue Jiang, Luke Richards, Zoe Schofield, Patrick Schäfer, Marco Polin, Orkun S Soyer, Munehiro Asally
{"title":"Emergence of synchronized growth oscillations in filamentous fungi.","authors":"Praneet Prakash, Xue Jiang, Luke Richards, Zoe Schofield, Patrick Schäfer, Marco Polin, Orkun S Soyer, Munehiro Asally","doi":"10.1098/rsif.2024.0574","DOIUrl":"10.1098/rsif.2024.0574","url":null,"abstract":"<p><p>Many species of soil fungi grow in the form of branched networks that enable long-range communication and mass flow of nutrient. These networks play important roles in the soil ecosystem as a major decomposer of organic materials. While there have been investigations on the branching of the fungal networks, their long-term growth dynamics in space and time is still not very well understood. In this study, we monitor the spatio-temporal growth dynamics of the plant-promoting filamentous fungus <i>Serendipita indica</i> for several days in a controlled environment within a microfluidic chamber. We find that <i>S. indica</i> cells display synchronized growth oscillations with the onset of sporulation and at a period of 3 h. Quantifying this experimental synchronization of oscillatory dynamics, we show that the synchronization can be recapitulated by the nearest neighbour Kuramoto model with a millimetre-scale cell-cell coupling. The microfluidic set-up presented in this work may aid the future characterization of the molecular mechanisms of the cell-cell communication, which could lead to biophysical approaches for controlling fungi growth and reproductive sporulation in soil and plant health management.</p>","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"21 219","pages":"20240574"},"PeriodicalIF":3.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11521610/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142546201","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Bingyang Zhang, Bishal Baskota, Philip S L Anderson
{"title":"Being thin-skinned can still reduce damage from dynamic puncture.","authors":"Bingyang Zhang, Bishal Baskota, Philip S L Anderson","doi":"10.1098/rsif.2024.0311","DOIUrl":"https://doi.org/10.1098/rsif.2024.0311","url":null,"abstract":"<p><p>The integumentary system in animals serves as an important line of defence against physiological and mechanical external forces. Over time, integuments have evolved layered structures (scales, cuticle and skin) with high toughness and strength to resist damage and prevent wound expansion. While previous studies have examined their defensive performance under low-rate conditions, the failure response and damage resistance of these thin layers under dynamic biological puncture remain underexplored. Here, we utilize a novel experimental framework to investigate the mechanics of dynamic puncture in both bilayer structures of synthetic tissue-mimicking composite materials and natural skin tissues. Our findings reveal the remarkable efficiency of a thin outer skin layer in reducing the overall extent of dynamic puncture damage. This enhanced damage resistance is governed by interlayer properties through puncture energetics and diminishes in strength at higher puncture rates due to rate-dependent effects in silicone tissue simulants. In addition, natural skin tissues exhibit unique material properties and failure behaviours, leading to superior damage reduction capability compared with synthetic counterparts. These findings contribute to a deeper understanding of the inherent biomechanical complexity of biological puncture systems with layered composite material structures. They lay the groundwork for future comparative studies and bio-inspired applications.</p>","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"21 219","pages":"20240311"},"PeriodicalIF":3.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11496953/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142502956","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Trade-offs and thermodynamics of energy-relay proofreading.","authors":"Jonas Berx, Karel Proesmans","doi":"10.1098/rsif.2024.0232","DOIUrl":"10.1098/rsif.2024.0232","url":null,"abstract":"<p><p>Biological processes that are able to discriminate between different molecules consume energy and dissipate heat, using a mechanism known as proofreading. In this work, we thoroughly analyse the thermodynamic properties of one of the most important proofreading mechanisms, namely Hopfield's energy-relay proofreading. We discover several trade-off relations and scaling laws between several kinetic and thermodynamic observables. These trade-off relations are obtained both analytically and numerically through Pareto optimal fronts. We show that the scheme is able to operate in three distinct regimes: an energy-relay regime, a mixed relay-Michaelis-Menten (MM) regime and a Michaelis-Menten regime, depending on the kinetic and energetic parameters that tune transitions between states. The mixed regime features a dynamical phase transition in the error-entropy production Pareto trade-off, while the pure energy-relay regime contains a region where this type of proofreading energetically outperforms standard kinetic proofreading.</p>","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"21 219","pages":"20240232"},"PeriodicalIF":3.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11461052/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142391530","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kevin J Painter, Valeria Giunta, Jonathan R Potts, Sara Bernardi
{"title":"Variations in non-local interaction range lead to emergent chase-and-run in heterogeneous populations.","authors":"Kevin J Painter, Valeria Giunta, Jonathan R Potts, Sara Bernardi","doi":"10.1098/rsif.2024.0409","DOIUrl":"10.1098/rsif.2024.0409","url":null,"abstract":"<p><p>In a chase-and-run dynamic, the interaction between two individuals is such that one moves towards the other (the chaser), while the other moves away (the runner). Examples can be found in both interacting cells and animals. Here, we investigate the behaviours that can emerge at a population level, for a heterogeneous group that contains subpopulations of chasers and runners. We show that a wide variety of patterns can form, from stationary patterns to oscillatory and population-level chase-and-run, where the latter describes a synchronized collective movement of the two populations. We investigate the conditions under which different behaviours arise, specifically focusing on the interaction ranges: the distances over which cells or organisms can sense one another's presence. We find that when the interaction range of the chaser is sufficiently larger than that of the runner-or when the interaction range of the chase is sufficiently larger than that of the run-population-level chase-and-run emerges in a robust manner. We discuss the results in the context of phenomena observed in cellular and ecological systems, with particular attention to the dynamics observed experimentally within populations of neural crest and placode cells.</p>","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"21 219","pages":"20240409"},"PeriodicalIF":3.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11522976/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142546207","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Escape motility of multicellular magnetotactic prokaryotes.","authors":"Xinyi Yang, Manu Prakash, Douglas R Brumley","doi":"10.1098/rsif.2024.0310","DOIUrl":"https://doi.org/10.1098/rsif.2024.0310","url":null,"abstract":"<p><p>Microorganisms often actively respond to multiple external stimuli to navigate toward their preferred niches. For example, unicellular magnetotactic bacteria integrate both oxygen sensory information and the Earth's geomagnetic field to help them locate anoxic conditions in a process known as magneto-aerotaxis. However, for multicellular magnetotactic prokaryotes (MMPs), the colonial structure of 4-16 cells places fundamental constraints on collective sensing, colony motility and directed swimming. To investigate how colonies navigate environments with multiple stimuli, we performed microfluidic experiments of MMPs with opposing magnetic fields and oxygen gradients. These experiments reveal unusual back-and-forth excursions called 'escape motility', in which colonies shuttle along magnetic field lines, punctuated by abrupt-yet highly coordinated-changes in collective ciliary beating. Through cell tracking and numerical simulations, we demonstrate that escape motility can arise through a simple magneto-aerotaxis mechanism, which includes the effect of magnetic torques and chemical sensing. At sufficiently high densities of MMPs, we observe the formation of dynamic crystal structures, whose stability is governed by the magnetic field strength and near-field hydrodynamic interactions. The results shed light on how some of the earliest multicellular organisms navigate complex physico-chemical landscapes.</p>","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"21 219","pages":"20240310"},"PeriodicalIF":3.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11480751/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142468783","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Michael Y Qiu, Charles B Suskin, Mohamed A Zayed, Guy M Genin, Joshua W Osbun
{"title":"Energy barriers govern catheter herniation during endovascular procedures: a 2.5D vascular flow model analysis.","authors":"Michael Y Qiu, Charles B Suskin, Mohamed A Zayed, Guy M Genin, Joshua W Osbun","doi":"10.1098/rsif.2024.0333","DOIUrl":"10.1098/rsif.2024.0333","url":null,"abstract":"<p><p>Endovascular procedures rely on navigating guidewires, catheters and other devices through tortuous vasculature to treat disease. A critical challenge in these procedures is catheter herniation, in which the device deviates from its intended path, often irrecoverably. To elucidate the mechanics of herniation, we developed a physical flow model of the aortic arch that enables direct measurement of device curvature during experimentally simulated neuroendovascular procedures conducted from an upper arterial access. Combined with measurements of initial, unstressed device shapes and flexural rigidities, the method enables the experimental estimation of the device bending energies during these simulated procedures. Characteristic energy profiles revealed distinct stages in both herniation and successful navigation, governed by the interplay between device properties and vascular anatomy. A deterministic progression from successful navigation to herniation was identified, with catheter systems following paths determined by measurable energy barriers. Increasing guidewire stiffness or decreasing catheter stiffness reduced the energy barrier for successful navigation while increasing that for herniation. This framework enables the prediction of endovascular herniation risk and offers unique insight into improved device design and clinical decision-making.</p>","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"21 219","pages":"20240333"},"PeriodicalIF":3.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11496950/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142502957","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
James Baxter, Ch Julián Villabona-Arenas, Robin N Thompson, Stéphane Hué, Roland R Regoes, Roger D Kouyos, Huldrych F Günthard, Jan Albert, Andrew Leigh Brown, Katherine E Atkins
{"title":"Reconciling founder variant multiplicity of HIV-1 infection with the rate of CD4<sup>+</sup> decline.","authors":"James Baxter, Ch Julián Villabona-Arenas, Robin N Thompson, Stéphane Hué, Roland R Regoes, Roger D Kouyos, Huldrych F Günthard, Jan Albert, Andrew Leigh Brown, Katherine E Atkins","doi":"10.1098/rsif.2024.0255","DOIUrl":"https://doi.org/10.1098/rsif.2024.0255","url":null,"abstract":"<p><p>HIV-1 transmission precipitates a stringent genetic bottleneck, with 75% of new infections initiated by a single genetic variant. Where multiple variants initiate infection, recipient set point viral load (SpVL) and the rate of CD4<sup>+</sup> T cell decline may be elevated, but these findings remain inconsistent. Here, we summarised the evidence for this phenomenon, then tested whether previous studies possessed sufficient statistical power to reliably identify a true effect of multiple variant infection leading to higher SpVL. Next, we combined models of HIV-1 transmission, heritability and disease progression to understand whether available data suggest a faster CD4<sup>+</sup> T cell decline would be expected to associated with multiple variant infection, without an explicit dependency between the two. First, we found that most studies had insufficient power to identify a true significant difference, prompting an explanation for previous inconsistencies. Next, our model framework revealed we would not expect to observe a positive association between multiple variant infections and faster CD4<sup>+</sup> T cell decline, in the absence of an explicit dependency. Consequently, while empirical evidence may be consistent with a positive association between multiple variant infection and faster CD4<sup>+</sup> T cell decline, further investigation is required to establish a causal basis.</p>","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"21 219","pages":"20240255"},"PeriodicalIF":3.7,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142546206","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Tautology explains evolution without variation and selection. A Comment on: 'An evolutionary process without variation and selection' (2021), by Gabora et al.","authors":"István Zachar,Jakab Máté,Szabolcs Számadó","doi":"10.1098/rsif.2023.0579","DOIUrl":"https://doi.org/10.1098/rsif.2023.0579","url":null,"abstract":"Gabora and Steel (Gabora L, Steel M. 2021 An evolutionary process without variation and selection. J. R. Soc. Interface 18, 20210334. [doi:10.1098/rsif.2021.0334]) claim that cumulative adaptive evolution is possible without natural selection, that is, without variation and competition. To support this claim, the authors modelled a theoretical process called self-other reorganization (SOR) that envisages a population of reflexively autocatalytic sets that can accumulate beneficial changes without any form of birth, death or selection, that is without population dynamics. The authors claim that despite being non-Darwinian, adaptive evolution happens in SOR, deeming it relevant to the origin of life and to cultural evolution. We analysed SOR and the claim that it implements evolution without variation and selection. We found that the authors, by design, ignore the growth and/or degradation of autocatalytic sets or their components, assuming all effects are beneficial and all entities in SOR are identical and immutable. We prove that due to these assumptions, SOR is a trivial model of horizontal percolation of beneficial effects over a static population. We implemented an extended model of SOR including more realistic assumptions to prove that accounting for any of the ignored processes inevitably leads to conventional Darwinian dynamics. Our analysis directly challenges the authors' claims, revealing evidence of an overly fragile foundation. While the best-case scenario the authors incorrectly generalize from may be mathematically valid, stripping away their unrealistic assumptions reveals that SOR does not represent real entities (e.g. protocells) but rather models the triviality that fast horizontal diffusion of effects can effectively equalize a population. Adaptation in SOR is solely because the authors only consider beneficial effects. The omission of death/growth dynamics and maladaptive effects renders SOR unrealistic and its relevance to evolution, cultural or biological, questionable.","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"18 1","pages":"20230579"},"PeriodicalIF":3.9,"publicationDate":"2024-09-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142262997","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Randall W Davis,Lorenzo Fiori,Bernd Würsig,Dara N Orbach
{"title":"Drag reduction and locomotory power in dolphins: Gray's paradox revealed.","authors":"Randall W Davis,Lorenzo Fiori,Bernd Würsig,Dara N Orbach","doi":"10.1098/rsif.2024.0227","DOIUrl":"https://doi.org/10.1098/rsif.2024.0227","url":null,"abstract":"For 88 years, biologists and engineers have sought to understand the hydrodynamics enabling dolphins to swim at speeds seemingly beyond their energetic capabilities, a phenomenon known as Gray's paradox. Hydromechanical models calculating the drag of swimming dolphins estimated power requirements for sustained high-speed swimming, which were physiologically impossible. Using an uncrewed aerial vehicle, we calculated the total power of free-ranging dusky dolphins (Lagenorhynchus obscurus) at speeds from 0.9 to 6.9 m s-1, deriving drag coefficients (Cd) and drag. Our results showed that the Cd decreased exponentially with speed, reducing drag by up to 89% at speeds >2 m s-1, with an additional 17% reduction during porpoising (>4.0 m s-1). At 6.9 m s-1, drag was 32 N, with a power of 15.8 W kg-1, nearly identical to the mass-specific allometric prediction for the maximum aerobic capacity of other mammals and physiologically possible. The Cd at speeds >2.5 m s-1 indicated reduced turbulence in the boundary layer around the dolphin's body, thereby reducing drag. The ability of dusky dolphins to swim at sustained high speeds resulted from an exponential decrease in Cd, which was further reduced by porpoising, thereby explaining the low drag and locomotory power that resolved Gray's paradox.","PeriodicalId":17488,"journal":{"name":"Journal of The Royal Society Interface","volume":"10 1","pages":"20240227"},"PeriodicalIF":3.9,"publicationDate":"2024-09-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142175239","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"综合性期刊","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}