Publications
publications by categories in reversed chronological order. generated by jekyll-scholar.
2025
- Salinity does not affect late-stage in-egg embryonic or immediate post-hatch development in an ecologically important land crab speciesLucy M Turner, Katharine A Clayton, Linn Wiberg, and 4 more authorsJournal of Experimental Biology, 2025
ABSTRACT Environmental drivers such as salinity can impact the timing and duration of developmental events in aquatic early life stages of crustaceans, including terrestrial crabs of the family Gecarcinidae. Low salinity delays larval development in land crabs, but nothing is known about its influence on the crucial late-stage encapsulated embryonic or immediate post-hatch development. Therefore, we exposed fertilised late-stage embryos of the Christmas Island red crab (Gecarcoidea natalis) to differing salinities (100%, 75%, 50% or 25% sea water) for 24 h during their spawning period and measured some key developmental and physiological traits. We found no effect of salinity on time of first heartbeat, time of hatching, first in-egg embryonic and post-hatch heart rate, or post-hatch activity duration. These results highlight the importance of considering all early life stages when fully characterising the effects of environmental drivers on crustacean development, including under climate change.
2024
- Dev-ResNet: automated developmental event detection using deep learningZiad Ibbini, Manuela Truebano, John I. Spicer, and 2 more authorsJournal of Experimental Biology, 2024
Delineating developmental events is central to experimental research using early life stages, permitting widespread identification of changes in event timing between species and environments. Yet, identifying developmental events is incredibly challenging, limiting the scale, reproducibility and throughput of using early life stages in experimental biology. We introduce Dev-ResNet, a small and efficient 3D convolutional neural network capable of detecting developmental events characterised by both spatial and temporal features, such as the onset of cardiac function and radula activity. We demonstrate the efficacy of Dev-ResNet using 10 diverse functional events throughout the embryonic development of the great pond snail, Lymnaea stagnalis. Dev-ResNet was highly effective in detecting the onset of all events, including the identification of thermally induced decoupling of event timings. Dev-ResNet has broad applicability given the ubiquity of bioimaging in developmental biology, and the transferability of deep learning, and so we provide comprehensive scripts and documentation for applying Dev-ResNet to different biological systems.
- LabEmbryoCam: An opensource phenotyping system for developing aquatic animalsZiad Ibbini, Maria Bruning, Sakina Allili, and 9 more authorsHardwareX, 2024
Phenomics is the acquisition of high-dimensional data on an individual-wide scale and is proving transformational in areas of biological research related to human health including medicine and the crop sciences. However, more broadly, a lack of accessible transferrable technologies and research approaches is significantly hindering the uptake of phenomics, in contrast to molecular-omics for which transferrable technologies have been a significant enabler. Aquatic embryos are natural models for phenomics, due to their small size, taxonomic diversity, ecological relevance, and high levels of temporal, spatial and functional change. Here, we present LabEmbryoCam, an autonomous phenotyping platform for timelapse imaging of developing aquatic embryos cultured in a multiwell plate format, and while optimised for embryos, the instrument is extremely versatile. The LabEmbryoCam capitalises on 3D printing, single board computers, consumer electronics and stepper motor enabled motion. We combine these into a compact and modular laboratory insturment to provide X, Y and Z motion of a camera and lens, a web application streamlined for rapid setup of experiments, user email notifications and a humidification chamber to reduce evaporation over prolonged acquisitions. Downstream analyses are provided, enabling automated embryo segmentation, heartrate measurement, motion tracking, and energy proxy trait (EPT) measurement. The LabEmbryoCam is a scalable, and flexible laboratory instrument, that leverages embryonic and early life stage organisms to tackle key global challenges including biological sensitivity assessment, toxicological screening, but also to support broader engagement with the earliest stages of life.
- Bioimaging and-the future of whole-organismal developmental physiologyOliver Tills, Ziad Ibbini, and John I. SpicerComparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 2024
While omics has transformed the study of biology, concomitant advances made at the level of the whole organism, i.e. the phenome, have arguably not kept pace with lower levels of biological organisation. In this personal commentary we evaluate the importance of imaging as a means of measuring whole organismal developmental physiology. Image acquisition, while an important process itself, has become secondary to image analysis as a bottleneck to the use of imaging in research. Here, we explore the significant potential for increasingly sophisticated approaches to image analysis, including deep learning, to advance our understanding of how developing animals grow and function. Furthermore, unlike many species-specific methodologies, tools and technologies, we explore how computer vision has the potential to be transferable between species, life stages, experiments and even taxa in which embryonic development can be imaged. We identify what we consider are six of the key challenges and opportunities in the application of computer vision to developmental physiology carried out in our lab, and more generally. We reflect on the tangibility of transferrable computer vision models capable of measuring the integrative physiology of a broad range of developing organisms, and thereby driving the adoption of phenomics for developmental physiology. We are at an exciting time of witnessing the move from computer vision as a replacement for manual observation, or manual image analysis, to it enabling a fundamentally more powerful approach to exploring and understanding the complex biology of developing organisms, the quantification of which has long posed a challenge to researchers.
2023
- Phenomics as an approach to Comparative Developmental PhysiologyJamie C. S. McCoy, John I. Spicer, Ziad Ibbini, and 1 more authorFrontiers in Physiology, 2023
The dynamic nature of developing organisms and how they function presents both opportunity and challenge to researchers, with significant advances in understanding possible by adopting innovative approaches to their empirical study. The information content of the phenotype during organismal development is arguably greater than at any other life stage, incorporating change at a broad range of temporal, spatial and functional scales and is of broad relevance to a plethora of research questions. Yet, effectively measuring organismal development, and the ontogeny of physiological regulations and functions, and their responses to the environment, remains a significant challenge. “Phenomics”, a global approach to the acquisition of phenotypic data at the scale of the whole organism, is uniquely suited as an approach. In this perspective, we explore the synergies between phenomics and Comparative Developmental Physiology (CDP), a discipline of increasing relevance to understanding sensitivity to drivers of global change. We then identify how organismal development itself provides an excellent model for pushing the boundaries of phenomics, given its inherent complexity, comparably smaller size, relative to adult stages, and the applicability of embryonic development to a broad suite of research questions using a diversity of species. Collection, analysis and interpretation of whole organismal phenotypic data are the largest obstacle to capitalising on phenomics for advancing our understanding of biological systems. We suggest that phenomics within the context of developing organismal form and function could provide an effective scaffold for addressing grand challenges in CDP and phenomics.
- Thermodynamic effects drive countergradient responses in the thermal performance of Littorina saxatilis across latitudeChristopher Dwane, Enrico L. Rezende, Oliver Tills, and 4 more authorsScience of The Total Environment, 2023
Thermal performance curves (TPCs) provide a powerful framework to assess the evolution of thermal sensitivity in populations exposed to divergent selection regimes across latitude. However, there is a lack of consensus regarding the extent to which physiological adjustments that compensate for latitudinal temperature variation (metabolic cold adaptation; MCA) may alter the shape of TPCs, including potential repercussion on upper thermal limits. To address this, we compared TPCs for cardiac activity in latitudinally-separated populations of the intertidal periwinkle Littorina saxatilis. We applied a non-linear TPC modelling approach to explore how different metrics governing the shape of TPCs varied systematically in response to local adaptation and thermal acclimation. Both critical upper limits, and the temperatures at which cardiac performance was maximised, were higher in the northernmost (cold-adapted) population and displayed a countergradient latitudinal trend which was most pronounced following acclimation to low temperatures. We interpret this response as a knock-on consequence of increased standard metabolic rate in high latitude populations, indicating that physiological compensation associated with MCA may indirectly influence variation in upper thermal limits across latitude. Our study highlights the danger of assuming that variation in any one aspect of the TPC is adaptive without appropriate mechanistic and ecological context.
- Comparative phenomics: a new approach to study heterochronyJamie C. S. McCoy, John I. Spicer, Simon D. Rundle, and 1 more authorFrontiers in Physiology, 2023
Understanding the links between development and evolution is one of the major challenges of biology. ‘Heterochronies’, evolutionary alterations in the timings of development are posited as a key mechanism of evolutionary change, but their quantification requires gross simplification of organismal development. Consequently, how changes in event timings influence development more broadly is poorly understood. Here, we measure organismal development as spectra of energy in pixel values of video, creating high-dimensional landscapes integrating development of all visible form and function. This approach we termed ‘Energy proxy traits’ (EPTs) is applied alongside previously identified heterochronies in three freshwater pulmonate molluscs (Lymnaea stagnalis, Radix balthica and Physella acuta). EPTs were calculated from time-lapse video of embryonic development to construct a continuous functional time series. High-dimensional transitions in phenotype aligned with major sequence heterochronies between species. Furthermore, differences in event timings between conspecifics were associated with changes in high-dimensional phenotypic space. We reveal EPTs as a powerful approach to considering the evolutionary importance of alterations to developmental event timings. Reimagining the phenotype as energy spectra enabled continuous quantification of developmental changes in high-dimensional phenotypic space, rather than measurement of timings of discrete events. This approach has the possibility to transform how we study heterochrony and development more generally.
- LabEmbryoCam: An opensource phenotyping system for developing aquatic animalsZiad Ibbini, Maria Bruning, Sakina Allili, and 5 more authorsbioRxiv, 2023
Phenomics is the acquisition of high-dimensional data on an individual-wide scale and is proving transformational in areas of biological research related to human health including medicine and the crop sciences. However, more broadly, a lack of available transferrable technologies and research approaches is significantly hindering the uptake of phenomics, in contrast to molecular-omics for which transferrable technologies have been a significant enabler. Aquatic embryos are natural models for phenomics, due to their small size, taxonomic diversity, ecological relevance, and high levels of temporal, spatial and functional change. Here, we present LabEmbryoCam, an autonomous phenotyping platform for timelapse imaging of developing aquatic embryos cultured in a multiwell plate format. The LabEmbryoCam capitalises on 3D printing, single board computers, consumer electronics and stepper motor enabled motion. These provide autonomous X, Y and Z motion, a web application streamlined for rapid setup of experiments, user email notifications and a humidification chamber to reduce evaporation over prolonged acquisitions. Downstream analyses are provided, enabling automated embryo segmentation, heartbeat detection, motion tracking, and energy proxy trait (EPT) measurement. LabEmbryoCam is a scalable, and flexible laboratory instrument, that leverages embryos and early life stages to tackle key global challenges including biological sensitivity assessment, toxicological screening and broader engagement with the earliest stages of life.
- A phenomics approach reveals interspecific differences in integrated developmental responses to chronic elevated temperaturesJamie C. S. McCoy, John I. Spicer, Simon D. Rundle, and 1 more authorJournal of Experimental Biology, 2023
Phenomics, high-dimensional organismal phenotyping, is advanced as a solution to quantifying complex developmental responses to elevated temperatures . ‘Energy proxy traits’ (EPTs) measure the phenotype as a spectrum of energy values across different temporal frequencies from pixel value fluctuations of video. Whilst they have proven effective in measuring the biology of complex and dynamic developing organisms, their utility in assessing environmental sensitivity of different species is untested. Using EPTs, we assess the relative thermal sensitivities of embryos of three species of freshwater snail with marked differences in their developmental event timings . Embryos of Lymnaea stagnalis, Radix balthica and Physella acuta were videoed hourly for the duration of their embryonic development at two temperatures: 20˚C and 25˚C. The video was used to calculate EPTs for the duration of their embryonic development, and during discrete physiological windows in development. Changes in energy spectra during development identified marked differences in thermal sensitivities between species, and suggest a relatively heightened sensitivity of gross rates of embryonic physiology and behaviour in embryos of R. balthica, developmental window specific thermal responses that reflect ontogenetic differences in observable physiologies, and temperature induced changes in physiological event timing. EPTs enabled comparison of high-dimensional spectral phenotypes, providing a unique capability for assessing sensitivity continuously in developing individuals. Such integrative and scalable phenotyping is prerequisite for improved understanding of the sensitivity of early life stages of different species.
- LabEmbryoCam: An opensource phenotyping system for developing aquatic animalsZiad Ibbini, Maria Bruning, Sakina Allili, and 5 more authorsbioRxiv, 2023
Phenomics is the acquisition of high-dimensional data on an individual-wide scale and is proving transformational in areas of biological research related to human health including medicine and the crop sciences. However, more broadly, a lack of available transferrable technologies and research approaches is significantly hindering the uptake of phenomics, in contrast to molecular-omics for which transferrable technologies have been a significant enabler. Aquatic embryos are natural models for phenomics, due to their small size, taxonomic diversity, ecological relevance, and high levels of temporal, spatial and functional change. Here, we present LabEmbryoCam, an autonomous phenotyping platform for timelapse imaging of developing aquatic embryos cultured in a multiwell plate format. The LabEmbryoCam capitalises on 3D printing, single board computers, consumer electronics and stepper motor enabled motion. These provide autonomous X, Y and Z motion, a web application streamlined for rapid setup of experiments, user email notifications and a humidification chamber to reduce evaporation over prolonged acquisitions. Downstream analyses are provided, enabling automated embryo segmentation, heartbeat detection, motion tracking, and energy proxy trait (EPT) measurement. LabEmbryoCam is a scalable, and flexible laboratory instrument, that leverages embryos and early life stages to tackle key global challenges including biological sensitivity assessment, toxicological screening and broader engagement with the earliest stages of life.
2022
- HeartCV: a tool for transferrable, automated measurement of heart rate and heart rate variability in transparent animalsZiad Ibbini, John I. Spicer, Manuela Truebano, and 2 more authorsJournal of Experimental Biology, 2022
Heart function is a key component of whole-organismal physiology. Bioimaging is commonly, but not exclusively, used for quantifying heart function in transparent individuals, including early developmental stages of aquatic animals, many of which are transparent. However, central limitations of many imaging-related methods is a lack of transferability between species, life-history stages and experimental approaches. Furthermore, locating the heart in mobile individuals remains challenging. Here, we present HeartCV: an open source Python package for automated measurement of heart rate and heart rate variability, that integrates automated localization and is transferrable across a wide range of species. We demonstrate the efficacy of HeartCV by comparing its outputs with measurements made manually for a number of very different species with contrasting heart morphologies. Lastly, we demonstrate the applicability of the software to different experimental approaches and to different dataset types, such as those corresponding to longitudinal data.
- Phenomics enables measurement of complex responses of developing animals to global environmental driversOliver Tills, Luke A. Holmes, Elliot Quinn, and 3 more authorsScience of The Total Environment, 2022
Phenomics offers technological advances for high-dimensional phenotyping, facilitating rapid, high-throughput assessment of physiological performance and has proven invaluable in global research challenges including drug discovery and food security. However, this rapidly growing discipline has remained largely inaccessible to the increasingly urgent challenge of assessing organismal functional sensitivity to global change drivers. Here, we investigate the response of an ecologically important marine invertebrate to multiple environmental drivers using Energy Proxy Traits (EPTs), a new approach for measuring complex phenotypes captured on video as a spectrum of energy levels across different temporal frequencies in fluctuating pixel values. We imaged three developmental stages of the common prawn Palaemon serratus at different salinities and temperatures, and measured EPTs and heart rate, a major proxy of physiological performance in ectotherms present across stages. Significant interactions were detected between temperature, developmental stage and salinity in frequency-specific energy levels. Despite cardiac activity being a significant contributor to the EPT spectra, treatment interactions were different from those observed on EPTs, highlighting additional phenotypic drivers of EPTs. Elevated temperature resulted in a shift of the EPT spectra towards higher frequency signals, indicating a reallocation of resources within the phenome. Using a non-linear dimensionality reduction, we interrogated the responses of EPT spectra in high-dimensional space. We discovered complex developmental-stage specific sensitivities, highlighting both the complexity of phenotypic responses, and the limits of using univariate approaches with pre-selected traits to assess responses to multiple global environmental drivers. EPTs are a high-dimensional, transferrable method of phenotyping, and are therefore highly relevant to addressing the current limitations of traditional methods of phenotyping applied to assessing biological sensitivity to drivers of global change. We predict that EPTs will become an important tool for indiscriminate phenotyping, transferrable between species, developmental stages and experimental designs.
2021
- Spectral phenotyping of embryonic development reveals integrative thermodynamic responsesOliver Tills, John I. Spicer, Ziad Ibbini, and 1 more authorBMC Bioinformatics, 2021
Energy proxy traits (EPTs) are a novel approach to high dimensional organismal phenotyping that quantify the spectrum of energy levels within different temporal frequencies associated with mean pixel value fluctuations from video. They offer significant potential in addressing the phenotyping bottleneck in biology and are effective at identifying lethal endpoints and measuring specific functional traits, but the extent to which they might contribute additional understanding of the phenotype remains unknown. Consequently, here we test the biological significance of EPTs and their responses relative to fundamental thermodynamic principles. We achieve this using the entire embryonic development of Radix balthica, a freshwater pond snail, at different temperatures (20, 25 & 30 °C) and comparing responses against predictions from Arrhenius’ equation (Q10 = 2). We find that EPTs are thermally sensitive and their spectra of frequency response enable effective high-dimensional treatment clustering throughout organismal development. Temperature-specific deviation in EPTs from thermodynamic predictions were evident and indicative of physiological mitigation, although they differed markedly in their responses from manual measures. The EPT spectrum was effective in capturing aspects of the phenotype predictive of biological outcomes, and suggest that EPTs themselves may reflect levels of energy turnover. Whole-organismal biology is incredibly complex, and this contributes to the challenge of developing universal phenotyping approaches. Here, we demonstrate the biological relevance of a new holistic approach to phenotyping that is not constrained by preconceived notions of biological importance. Furthermore, we find that EPTs are an effective approach to measuring even the most dynamic life history stages.
- Divergence in Thermal Physiology Could Contribute to Vertical Segregation in Intertidal Ecotypes of Littorina saxatilisChristopher Dwane, Simon D Rundle, Oliver Tills, and 4 more authorsPhysiological and Biochemical Zoology, 2021
AbstractThermal stress is a potentially important selective agent in intertidal marine habitats, but the role that thermal tolerance might play in local adaptation across shore height has been underexplored. Northwest Spain is home to two morphologically distinct ecotypes of the periwinkle Littorina saxatilis, separated by shore height and subject to substantial differences in thermal stress exposure. However, despite other biotic and abiotic drivers of ecotype segregation being well studied, their thermal tolerance has not been previously characterized. We investigated thermal tolerance across multiple life history stages by employing the thermal death time (TDT) approach to determine (i) whether the two ecotypes differ in thermal tolerance and (ii) how any differences vary with life history stage. Adults of the two ecotypes differed in their thermal tolerance in line with their shore position: the upper-shore ecotype, which experiences more extreme temperatures, exhibited greater endurance of thermal stress compared with the lower-shore ecotype. This difference was most pronounced at the highest temperatures tested. The proximate physiological basis for these differences is unknown but likely due to a multifarious interaction of traits affecting different parts of the TDT curve. Differences in tolerance between ecotypes were less pronounced in early life history stages but increased with ontogeny, suggesting partial divergence of this trait during development. Thermal tolerance could potentially play an important role in maintaining population divergence and genetic segregation between the two ecotypes, since the increased thermal sensitivity of the lower-shore ecotype may limit its dispersal onto the upper shore and so restrict gene flow.
2020
- Both maternal and embryonic exposure to mild hypoxia influence embryonic development of the intertidal gastropod Littorina littoreaJames C. S. McCoy, John I. Spicer, Oliver Tills, and 1 more authorJournal of Experimental Biology, 2020
There is growing evidence that maternal exposure to environmental stressors can alter offspring phenotype and increase fitness. Here, we investigate the relative and combined effects of maternal and developmental exposure to mild hypoxia (65 and 74% air saturation, respectively) on the growth and development of embryos of the marine gastropod Littorina littorea. Differences in embryo morphological traits were driven by the developmental environment, whereas the maternal environment and interactive effects of maternal and developmental environment were the main driver of differences in the timing of developmental events. While developmental exposure to mild hypoxia significantly increased the area of an important respiratory organ, the velum, it significantly delayed hatching of veliger larvae and reduced their size at hatching and overall survival. Maternal exposure had a significant effect on these traits, and interacted with developmental exposure to influence the time of appearance of morphological characters, suggesting that both are important in affecting developmental trajectories. A comparison between embryos that successfully hatched and those that died in mild hypoxia revealed that survivors exhibited hypertrophy in the velum and associated pre-oral cilia, suggesting that these traits are linked with survival in low-oxygen environments. We conclude that both maternal and developmental environments shape offspring phenotype in a species with a complex developmental life history, and that plasticity in embryo morphology arising from exposure to even small reductions in oxygen tensions affects the hatching success of these embryos.
2019
- Moderate reductions in dissolved oxygen may compromise performance in an ecologically-important estuarine invertebrateMichael Collins, Oliver Tills, Lucy M Turner, and 3 more authorsScience of The Total Environment, 2019
2018
- A high-throughput and open-source platform for embryo phenomics.Oliver Tills, John I Spicer, Andrew Grimmer, and 4 more authorsPLoS Biology, 2018
Phenomics has the potential to facilitate significant advances in biology but requires the development of high-throughput technologies capable of generating and analysing high-dimensional data. There are significant challenges associated with building such technologies, not least those required for investigating dynamic processes such as embryonic development, during which high rates of temporal, spatial, and functional change are inherently difficult to capture. Here, we present EmbryoPhenomics, an accessible high-throughput platform for phenomics in aquatic embryos comprising an Open-source Video Microscope (OpenVIM) that produces high-resolution videos of multiple embryos under tightly controlled environmental conditions. These videos are then analysed by the Python package Embryo Computer Vision (EmbryoCV), which extracts phenomic data for morphological, physiological, behavioural, and proxy traits during the process of embryonic development. We demonstrate the broad-scale applicability of EmbryoPhenomics in a series of experiments assessing chronic, acute, and multistressor responses to environmental change (temperature and salinity) in >30 million images of >600 embryos of two species with markedly different patterns of development-the pond snail Radix balthica and the marine amphipod Orchestia gammarellus. The challenge of phenomics is significant but so too are the rewards, and it is particularly relevant to the urgent task of assessing complex organismal responses to current rates of environmental change. EmbryoPhenomics can acquire and process data capturing functional, temporal, and spatial responses in the earliest, most dynamic life stages and is potentially game changing for those interested in studying development and phenomics more widely.
- Thermal strategies vary with life history stage.Manuela Truebano, Phillip Fenner, Oliver Tills, and 2 more authorsThe Journal of experimental biology, Apr 2018
With both global surface temperatures and the incidence and intensity of extreme temperature events projected to increase, the assessment of species’ sensitivity to chronic and acute changes in temperature has become crucial. Sensitivity predictions are based predominantly on adult responses, despite the fact that early life stages may be more vulnerable to thermal challenge. Here, we compared the sensitivity of different life history stages of the intertidal gastropod Littorina obtusatausing thermal death time curves, which incorporate the intensity and duration of heat stress, and used these to calculate upper critical thermal limits (CTmax) and sensitivity to temperature change (z). Early (larval) life stages had both a lower CTmaxand a lower zthan adults, suggesting they are less good at withstanding short-term extreme thermal challenges but better able to survive moderate temperatures in the long term. This result supports the predicted trade-off between acute and chronic tolerance to thermal stress, and is consistent with the different thermal challenges that these stages encounter in the intertidal zone. We conclude that different life history stages employ different thermal strategies that may be adaptive. Our findings caution against the use of predictions of the impact of global warming that are based on only adult responses and, hence, which may underestimate vulnerability.
- Transcriptomic responses to predator kairomones in embryos of the aquatic snail Radix balthicaOliver Tills, Manuela Truebano, Barbara Feldmeyer, and 4 more authorsEcology and Evolution, Oct 2018
The ability of organisms to respond to predation threat by exhibiting induced defenses is well documented, but studies on the potential mechanistic basis for such responses are scarce. Here, we examine the transcriptomic response to predator kairomones of two functionally distinct developmental stages in embryos of the aquatic snail Radix balthica: E8—the stage at which a range‐finding trial indicated that kairomone‐induced accelerated growth and development first occurred; and E9—the stage at which embryos switched from ciliary‐ to crawling‐driven locomotion. We tested whether expression profiles were influenced by kairomones and whether this influence varied between stages. We also identified potential candidate genes for investigating mechanisms underpinning induced responses. There were 6,741 differentially expressed transcripts between developmental stages, compared to just five in response to predator kairomones. However, on examination of functional enrichment in the transcripts responding to predator kairomones and adopting a less stringent significance threshold, 206 transcripts were identified relating to muscle function, growth, and development, with this response being greater at the later E9 stage. Furthermore, these transcripts included putative annotations for genes identified as responding to predator kairomones in other taxa, including C1q, lectin, and actin domains. Globally, transcript expression appeared reduced in response to predator kairomones and we hypothesize that this might be a result of metabolic suppression, as has been reported in other taxa in response to predation threat. We describe molecular responses to predatory fish kairomone occurring at functionally distinct embryonic stages in a freshwater pond snail. We identify molecular responses indicative of accelerated growth, muscle function, and shell development, and these were responses that were also observed at the phenotypic level.
- Transcriptomic responses to predator kairomones in embryos of the aquatic snail Radix balthicaOliver Tills, Manuela Truebano, Barbara Feldmeyer, and 4 more authorsEcology and Evolution, Oct 2018
The ability of organisms to respond to predation threat by exhibiting induced defenses is well documented, but studies on the potential mechanistic basis for such responses are scarce. Here, we examine the transcriptomic response to predator kairomones of two functionally distinct developmental stages in embryos of the aquatic snail Radix balthica: E8—the stage at which a range‐finding trial indicated that kairomone‐induced accelerated growth and development first occurred; and E9—the stage at which embryos switched from ciliary‐ to crawling‐driven locomotion. We tested whether expression profiles were influenced by kairomones and whether this influence varied between stages. We also identified potential candidate genes for investigating mechanisms underpinning induced responses. There were 6,741 differentially expressed transcripts between developmental stages, compared to just five in response to predator kairomones. However, on examination of functional enrichment in the transcripts responding to predator kairomones and adopting a less stringent significance threshold, 206 transcripts were identified relating to muscle function, growth, and development, with this response being greater at the later E9 stage. Furthermore, these transcripts included putative annotations for genes identified as responding to predator kairomones in other taxa, including C1q, lectin, and actin domains. Globally, transcript expression appeared reduced in response to predator kairomones and we hypothesize that this might be a result of metabolic suppression, as has been reported in other taxa in response to predation threat.
- Developmental Plasticity and HeterokairyJohn Spicer, Oliver Tills, Manuela Truebano, and 1 more authorIn Development and Evolution, Oct 2018
2017
- An Annotated Draft Genome for Radix auricularia (Gastropoda, Mollusca)Tilman Schell, Tilman Schell, Barbara Feldmeyer, and 12 more authorsGenome Biology and Evolution, Mar 2017
2016
- Reduced pH affects pulsing behaviour and body size in ephyrae of the moon jellyfish, Aurelia auritaO Tills, X Sun, S D Rundle, and 6 more authorsJournal of Experimental Marine Biology and Ecology, Jul 2016
Journal of Experimental Marine Biology and Ecology, 480 (2016) 54-61. doi:10.1016/j.jembe.2016.03.014
- Embryonic transcriptome of the brackishwater amphipod Gammarus chevreuxi.Manuela Truebano, Oliver Tills, and John I SpicerMarine Genomics, Jul 2016
Environmental change can dramatically alter the development of aquatic organisms. While the effect of such change on physiological and morphological ontogenies is becoming clearer, the molecular mechanisms underpinning them are largely unexplored. Characterizing these mechanisms is often limited by the lack of molecular resources. We have applied Illumina HiSeq sequencing to RNA isolated from different developmental stages of the brackishwater amphipod Gammarus chevreuxi. Over 52.6M paired-end reads were assembled de novo into 172,081 contigs, representing 118,812 potential genes. The assembly generated constitutes a reference embryonic transcriptome for an ecologically-important aquatic shredder species. This resource will contribute to our understanding of the mechanisms underpinning the development of physiological function through functional, comparative and quantitative expression studies. It will also allow the identification of candidate biomarkers for assessing the impact of environmental stressors in estuarine systems.
2015
- An embryonic transcriptome of the pulmonate snail Radix balthica.Oliver Tills, Manuela Truebano, and Simon D RundleMarine Genomics, Jul 2015
The pond snail, Radix balthica (Linnaeus 1758), is an emerging model species within ecological developmental biology. While its development has been characterised in detail, genomic resources for embryonic stages are lacking. We applied Illumina MiSeq RNA-seq to RNA isolated from pools of embryos at two points during development. Embryos were cultured in either the presence or absence of predator kariomones to increase the diversity of the transcripts assembled. Sequencing produced 47.2M paired-end reads, assembled into 54,360 contigs of which 73% were successfully annotated. This transcriptome provides an invaluable resource to build a mechanistic understanding of developmental plasticity.
2014
- Combining motion analysis and microfluidics–a novel approach for detecting whole-animal responses to test substances.Tabitha S Rudin-Bitterli, Oliver Tills, John I Spicer, and 4 more authorsPloS one, Jul 2014
Small, early life stages, such as zebrafish embryos are increasingly used to assess the biological effects of chemical compounds in vivo. However, behavioural screens of such organisms are challenging in terms of both data collection (culture techniques, drug delivery and imaging) and data evaluation (very large data sets), restricting the use of high throughput systems compared to in vitro assays. Here, we combine the use of a microfluidic flow-through culture system, or BioWell plate, with a novel motion analysis technique, (sparse optic flow - SOF) followed by spectral analysis (discrete Fourier transformation - DFT), as a first step towards automating data extraction and analysis for such screenings. Replicate zebrafish embryos housed in a BioWell plate within a custom-built imaging system were subject to a chemical exposure (1.5% ethanol). Embryo movement was videoed before (30 min), during (60 min) and after (60 min) exposure and SOF was then used to extract data on movement (angles of rotation and angular changes to the centre of mass of embryos). DFT was subsequently used to quantify the movement patterns exhibited during these periods and Multidimensional Scaling and ANOSIM were used to test for differences. Motion analysis revealed that zebrafish had significantly altered movements during both the second half of the alcohol exposure period and also the second half of the recovery period compared to their pre-treatment movements. Manual quantification of tail flicking revealed the same differences between exposure-periods as detected using the automated approach. However, the automated approach also incorporates other movements visible in the organism such as blood flow and heart beat, and has greater power to discern environmentally-driven changes in the behaviour and physiology of organisms. We suggest that combining these technologies could provide a highly efficient, high throughput assay, for assessing whole embryo responses to various drugs and chemicals.
2013
- A novel application of motion analysis for detecting stress responses in embryos at different stages of developmentOliver Tills, Tabitha Bitterli, Phil Culverhouse, and 2 more authorsBMC Bioinformatics, Jul 2013
BMC Bioinformatics 2013, 14:1. doi:10.1186/1471-2105-14-37
- Parent-offspring similarity in the timing of developmental events: an origin of heterochrony?Oliver Tills, Simon D Rundle, and John I SpicerProceedings. Biological sciences / The Royal Society, Oct 2013
Understanding the link between ontogeny (development) and phylogeny (evolution) remains a key aim of biology. Heterochrony, the altered timing of developmental events between ancestors and descendants, could be such a link although the processes responsible for producing heterochrony, widely viewed as an interspecific phenomenon, are still unclear. However, intraspecific variation in developmental event timing, if heritable, could provide the raw material from which heterochronies originate. To date, however, heritable developmental event timing has not been demonstrated, although recent work did suggest a genetic basis for intraspecific differences in event timing in the embryonic development of the pond snail, Radix balthica. Consequently, here we used high-resolution (temporal and spatial) imaging of the entire embryonic development of R. balthica to perform a parent-offspring comparison of the timing of twelve, physiological and morphological developmental events. Between-parent differences in the timing of all events were good predictors of such timing differences between their offspring, and heritability was demonstrated for two of these events (foot attachment and crawling). Such heritable intraspecific variation in developmental event timing could be the raw material for speciation events, providing a fundamental link between ontogeny and phylogeny, via heterochrony.
- Variance in developmental event timing is greatest at low biological levels: implications for heterochronyOliver Tills, Simon D Rundle, and John I SpicerBiological Journal of the Linnean Society, Sep 2013
Variation is the raw material required for natural selection to operate (Darwin, 1859) and understanding the nature of variation in physiological, morphological, developmental, and behavioural traits is key to understanding ecology and evolution (Spicer & Gaston, 1999; ...
2011
- Studying the altered timing of physiological events during development: It’s about time - or is it?John I Spicer, Simon D Rundle, and Oliver TillsRespiratory physiology & neurobiology, Sep 2011
The investigation of the altered timing of developmental events is key to understanding evolution. Most empirical investigations of event timing are biased towards studying morphological variation. Recent reviews, however, have attempted to marshal the evidence for the importance of altered timing of physiological events, focusing on such timing shifts between species (physiological heterochrony) and within species (physiological heterokairy). Here we update these reviews. We firstly take a comparative developmental physiology approach to explore how recent studies have furthered our understanding of the links between physiological event timing shifts at different levels of biological organisation (i.e. individual, population and species). The alternative strategy of concentrating effort on one model system is then considered, in particular focussing on substantial recent advances in our understanding of fetal haemoglobin expression in humans. We conclude that, while the fetal haemoglobin model may be appropriate as a model for some questions, it can never be the model study system. We also discuss the different quantitative analyses available for investigating event timing alterations. We consider the efficacy of the terms heterochrony and heterokairy.
- A genetic basis for intraspecific differences in developmental timing?Oliver Tills, Simon D. Rundle, Moritz Salinger, and 3 more authorsEvolution & Development, Sep 2011
Heterochrony, altered developmental timing between ancestors and their descendents, has been proposed as a pervasive evolutionary feature and recent analytical approaches have confirmed its existence as an evolutionary pattern. Yet, the mechanistic basis for heterochrony remains unclear and, in particular, whether intraspecific variation in the timing of developmental events generates, or has the potential to generate, future between‐species differences. Here we make a key step in linking heterochrony at the inter‐ and intraspecific level by reporting an association between interindividual variation in both the absolute and relative timing (position within the sequence of developmental events) of key embryonic developmental events and genetic distance for the pond snail, Radix balthica. We report significant differences in the genetic distance of individuals exhibiting different levels of dissimilarity in their absolute and relative timing of developmental events such as spinning activity, eyespot formation, heart ontogeny, and hatching. This relationship between genetic and developmental dissimilarity is consistent with there being a genetic basis for variation in developmental timing and so suggests that intraspecific heterochrony could provide the raw material for natural selection to produce speciation.
2010
- Salinity-induced heterokairy in an upper-estuarine population of the snail Radix balthica (Mollusca: Pulmonata)O Tills, JI Spicer, and SD RundleAquatic Biology, Sep 2010