Does developmental plasticity influence speciation?

Lead Research Organisation: University of Southampton
Department Name: Sch of Ocean and Earth Science

Abstract

Life is a journey. As we grow older, we change. Sometimes we respond in the spur of the moment. Occasionally, an event has long-lasting consequences in spite of any change in circumstance and shapes our outlook far into the future.

This future flexibility, or a lack thereof, also applies to the traits like size and weight that influence our daily risk of death and our reproductive success. Some of these traits retain flexibility throughout life, whereas others can only change in a fixed early window. As humans, we are far more likely to shift weight gain trajectories before six months of age than when older.

Any ability to flexibly adjust traits can boost survival chances in new or changing environments, but also provides the means to innovate and so express new combinations of traits. Flexibility as a means of innovation might promote the divergence of ancestral organisms into new species, but also might not because such flexibility would mean that species can already deal with whatever circumstances they encounter, which would in turn remove the pressure for any innovation to become hardwired into their DNA.

The long timescales over which this hardwiring plays out complicates collection of data. We don't know whether future flexibility or a lack of it is more likely to catalyse change into new species. In this project, we will contribute this increasingly requested data and therefore provide the first evidence if a lifetime of flexibility, or a stubborn refusal to change, influences the emergence of new species.

Planktonic foraminifera are single-celled organisms that live in vast numbers in all the world's oceans. While chemical analysis of their fossil remains has generated a remarkably continuous record of past climate change, each individual also retains a complete record of its size and shape at each stage along its journey through life.

These growth stages can be revealed by state-of-the-art imaging technology, which has sparked a digital revolution in how biologists study life on Earth. To study evolution, we need to study differences among lots of individuals. We need to know how and why these differences change through time. This need to measure lots of individuals means that the current practise of a person pointing and clicking on a computer screen to identify distinct parts is too slow. Computer programmes that provide a faster, more repeatable and less biased way of identifying and analysing such parts are now available, completing the toolkit needed to build big databases.

By bringing together lessons from diverse scientific disciplines, we propose to use the same fossil specimens to collate records of an individual's journey through life and the environment it experienced every step of the way, both of which were changing from day-to-day, millions of years ago.

While the fossil record of planktonic foraminifera provides the necessary timespan and abundance, new computer programmes and imaging technology complete the toolkit jigsaw to investigate for the first time if certain parts of an individual's journey through life are more influential than others in determining the eventual evolutionary destinations of its species.

Our unique, direct link between organism and environment lets us study the dynamic journey through life in the static death of the fossil record. The fundamental limitation to the current ways we study how new species emerge is the lack of repeated samples through time to follow the genesis of novel lifeforms, and explicitly targeting this limitation using state-of-the-art approaches from multiple scientific disciplines means we will deliver a breakthrough in attempts to answer one of the most fundamental of all biological questions: how do differences among individuals make differences among species?

Planned Impact

PISTON takes an unprecedented transdisciplinary approach to investigate how new species form. Species are the foundation of biodiversity. The House of Lords Systematics & Taxonomy review identified biodiversity's critical underpinning of an extensive array of natural environment research ranging from blue skies evolutionary questions, particularly into charismatic "missing links" that reveal how differences among individuals generate differences among species, to applied questions such as ecosystem service provision (i.e., the benefits we derive from natural ecosystems) and global health threat mitigation.

PISTON has been designed as a set of interrelated work packages that will integrate to more than the sum of their individual parts to impact policy, public health, industry and the general public. PISTON investigators are active in all these sectors and will build on and further develop existing relationships and activities.

Members of PISTON have a strong track record of contributing to Intergovernmental Panel on Climate Change (IPCC) reports. Our unprecedented data, focusing on the pivotal link between organism and environment and from the last interval when the world was 2-3 degrees warmer than it is today, can contribute to future IPCC reports in this area. Foster (Contributing Author) and Schmidt (Chapter Lead Author; Co-author of Summary for Policymakers) will co-ordinate impact in this area.

Proprietary versions of WP1 computer vision algorithms have successfully delineated the ball and socket of hip joints as a diagnostic to improve hip replacement therapy, which indicates their potential for wider healthcare benefits for the general public. The PISTON team has considerable experience working with industry (Sinclair with Nikon to develop bespoke biological and medical tools) and the public sector (Nixon on, e.g., automated gait recognition) and will draw on this experience to ensure the open-source PISTON outputs are carefully described, annotated and made accessible in toolbox form to the broadest possible community of end-users.

Taxonomic revisions through refined dating and age control will directly impact foraminiferal specialists in commercial operations, particularly the oil industry. The statistical approaches we propose minimise subjective choices, which adds repeatability and transparency across end-users. We will build on existing networks: Wade (NE/N017900) and Wilson (PI: NE/K007211 and NE/K014137) name PetroStrat, Network Stratigraphic, Shell, RPS Energy and Neftex-Halliburton as Industrial Partners on current awards. Wade will act as Industry Impact Champion (1.5% costed time) to incorporate PISTON data and curate the Mikrotax illustrated online portal. In addition to working with External Advisory Board member Haydon Bailey (Network Stratigraphic) to deliver Industrial impact, we will invite further industrial partners to the second scientific scoping workshop in Year 3 (£2500 budgeted for one UK and one international).

All Research Staff will participate in Public Engagement activities during PISTON in areas of particular appeal to each individual. In particular, we will work with Ellen Dowell, a Science Communicator, interdisciplinary facilitator and current collaborator of PI Ezard (NE/J018163), to run interactive workshops in Einstein's Garden at the Green Man Festival in Year 3 (led by Aze), which we will then run subsequently at exhibitions through applications to the NERC Science Festival, Royal Society Summer School and local science festivals in our regions. These hands-on workshops will let festival-goers see evolution in action and contribute to an animated "flick book" style-film based on the divergence into new species (£3000 budgeted). This film will ensure legacy and impact beyond the festival fence.

Publications

10 25 50
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Bataillon T (2022) Genetics of adaptation and fitness landscapes: From toy models to testable quantitative predictions. in Evolution; international journal of organic evolution

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Fabbrini A (2021) Systematic taxonomy of middle Miocene Sphaeroidinellopsis (planktonic foraminifera) in Journal of Systematic Palaeontology

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Searle-Barnes A (2023) Laser ablation mass spectrometry blast through detection in R. in Rapid communications in mass spectrometry : RCM

Studentship Projects

Project Reference Relationship Related To Start End Student Name
NE/P019269/1 02/10/2017 01/10/2023
2383703 Studentship NE/P019269/1 01/03/2018 01/09/2021 Laura Mears
2570968 Studentship NE/P019269/1 01/10/2021 31/03/2025 James Mulqueeney
 
Description PISTON is a transdisciplinary proposal addressing one of the most fundamental of all biological questions: how does variation among individuals generate variation among species? Reviewers described it as "truly ground-breaking in its detail, quality and ambition". Within UoS, I have built new collaborations among Engineers, Computer Scientists, Geochemists and Biologists. We have developed high-throughput repeatable protocols on Synchrotron-equivalent volumetric micro-tomography and laser ablation inductively coupled plasma mass spectrometry. The datasets we have built are already an order of magnitude larger than anything else in the world and ready for analysis into PISTON's scientific questions. My research vision remains to integrate interdisciplinary academic excellence wherever it may be.

As for many researchers, the most recent submission period has presented severe challenges. As PI, I am Clinically Extremely Vulnerable and so have lent heavily on my team to continue delivering the integrated datasets. The most obvious example of disruption is that we were running stable isotope samples in Ocean & Earth Science's (OES) Organic Geochemistry Facility, part of the SEAPORT Carbon Laboratories, when we went into lockdown 1 and that batch of samples were completed in October 2020. The upgrade of the OES ICP-MS system to a Triple Quad ICP-MS required substantial remote troubleshooting of hard- and software. In autumn 2021, we revised our analytical processing steps to a fully automated end-to-end process that enables the throughput that PISTON requires. These processing steps offer improved methodology for all ICP-MS data as well as bespoke workflows for the UoS system, which will benefit researchers beyond the immediate project (the open-source application on foraminifera and coral case studies is now under review). Those software packages are either published in open source outlets or in review, as well as being accessible on github. Data collection is now substantively complete - the iterative nature of the project has meant we have obtained more data than originally intended, albeit on fewer total individuals overall, but this follows the discovery of key new results (now published) of more variation through ontogeny than across subspecies; this result is central to the research focus and we therefore adapted our methodological approach to ensure sufficient statistical power to stand the best chance of answering our research questions. We have the largest intraspecific x-ray CT and LA-ICP-MS datasets that we are aware of in the world, as well as the means to link them together to answer our core questions. The abundance of these data pose fundamental geochemical questions on interpretation, which has been the major focus of recent months work. Having run a number of diagnostic checks on those geochemical data, we are confident in their repeatability and our analytical workflow and various sensitivity analyses we have undertaken are now all available.

We have more publications in later rounds of peer review and anticipate growing levels of outputs through the fully integrated morphological and geochemical datasets. These outputs are delayed due to various COVID related pressures. Having completed the data collation pipeline and run statistical models to verify the meaning of our results, the major tasks now are to complete the publication of key results to answer the grant's focal questions. 6 Team Members attended the Geological Society of America's meeting in Denver in October 2022 to present these results and gather feedback from the community. We continue to contribute to community efforts and working groups in both palaeocological and taxonomic realms to ensure our findings have the largest community impact.
Exploitation Route Software is currently being developed under open-source (R) and proprietary licenses (MATLAB), but is planned to be converted to fully reproducible platforms later. We are settled on an optimal set of statistical outputs from the feature extraction algorithms, all of which will be released in a holistic view of open science. The appointment in December 2020 of PDRF Meng to the remainder of the role initially filled by PDRF Zhang has catalysed this process. PDRF Brombacher (morphometric 3d coiling spires from x-ray CT images) has published her open-source R package and RA Searle-Barnes (improved methodology for processing the LA-ICP-MS data) has submitted his open-source R package for peer review. Development versions remain on Github.
Sectors Digital/Communication/Information Technologies (including Software),Education,Culture, Heritage, Museums and Collections,Security and Diplomacy

URL https://www.southampton.ac.uk/oes/research/projects/piston-does-developmental-plasticity-influence-speciation.page
 
Description In very early stages of development work with De La Rue for use of high-resolution computed tomographic images to be used in passport and banknote security features. Julian Payne (Creative Director), Andy Sharp (Photographer) and Stuart Rost (Designer) from De La Rue visited in September 2018 to discuss plans, capture images and talk to team members. The final developed work used other images but the methodology was inspired by those captured in this project. Images became part of a National Trust exhibition on digital nature from May 2019; precise involvement to be clarified and led by University of Bristol component of the award. In 2019, working with colleagues in the University of Southampton's IT department, we developed a fully interactive Virtual Reality experience "climbing" inside the shells of these plankton to crawl back through their life histories to the earliest stages of development that are some 15 um in diameter. We have beta-tested the experience with 3rd year undergraduate students within the Microfossils, Environments, Evolution and Time module at the University of Southampton and will roll out related public engagement activities based on these experiences in the post-COVID world. Ezard is now a member of the University-wide Virtual Reality Special Interest Group co-ordinating the best ways to develop such features across a Research, Education and Enterprise portfolio.
First Year Of Impact 2018
Sector Digital/Communication/Information Technologies (including Software),Education,Culture, Heritage, Museums and Collections,Security and Diplomacy
Impact Types Cultural,Societal

 
Description Improving Digital Security features on passports and banknotes
Geographic Reach Local/Municipal/Regional 
Policy Influence Type Influenced training of practitioners or researchers
Impact The x-ray CT images we have developed were used by digital security firm De La Rue to update their digital security features. As we have built the largest collection of intraspecific variation x-ray CT scans (by an order of magnitude), we have many similar images with fine scale variation in micro-morphological features. This natural variation in the porosity of plankton makes bank notes and passports exceptionally difficult to forge when these images are used as backdrops. De La Rue Creative Director Julian Payne wrote "without your involvement we would not have focussed on the University of Southampton." The final prototypes used medical imagery rather than our plankton for ease of communication with stakeholders (i.e. De La Rue customers), but we were a crucial stage in the Research and Development phase.
 
Description Discipline Hopping Scheme
Amount £29,235 (GBP)
Organisation University of Southampton 
Sector Academic/University
Country United Kingdom
Start 01/2022 
End 03/2022
 
Description Lorna Kearns' Doctoral Enhancement Award
Amount $15,000 (USD)
Organisation The Cushman Foundation 
Sector Charity/Non Profit
Country United States
Start 11/2021 
End 06/2022
 
Description The contribution of plasticity to adaptive divergence: domestication as a model
Amount £473,142 (GBP)
Funding ID NE/S002022/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 01/2019 
End 12/2021
 
Description Understanding of diachroneity: Palaeoenvironmental controls on dispersal of planktic foraminifera in the Plio-Pleistocene oceans
Amount £50,496 (GBP)
Funding ID NE/T012382/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 05/2019 
End 04/2022
 
Title Data from: Small but mighty: how overlooked small species maintain community structure through middle Eocene climate change 
Description Understanding current and future biodiversity responses to changing climate is pivotal as anthropogenic climate change continues. This understanding is complicated though by the multitude of available metrics to quantify dynamics, and by biased sampling protocols. Here, we investigate the impact of sampling protocol strategies using a data-rich fossil record to calculate effective diversity using Hill numbers for the first time on Paleogene planktonic foraminifera. We sample 22,830 individual tests, in two different size classes, across a seven-million-year time slice of the Middle Eocene featuring a major transient warming event, the Middle Eocene Climatic Optimum (MECO; ~40 million years ago (Ma)), at study sites in the mid-latitude North Atlantic. Using Generalized Additive Models (GAMs), we investigate community responses to climatic fluctuations. After correcting for any effects of fossil fragmentation, we show a peak in generic diversity in the early and mid-stages of the MECO as well as divergent trajectories between the typical size-selected community (> 180 µm) and a broader selection including smaller genera (> 63 µm). Assemblages featuring smaller genera are more resilient to the climatic fluctuations of the MECO than those assemblages that feature only larger genera, maintaining their community structure at the reference Hill numbers for Shannon's and Simpson's Index. These results raise fundamental questions about how communities respond to climate excursions. In addition, our results emphasise the need to design studies with the aim of collecting the most inclusive data possible, to allow detection of community changes and determine which species are likely to dominate future environments. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.cfxpnvx81
 
Title Data sets for 'The influence of geochemical variation among Globigerinoides ruber individuals on paleoceanographic reconstructions' 
Description This dataset contains geochemical and morphological data for the planktic foraminifera Globigerinoides ruber. Descriptions of data can be found in the ReadME file and in the realted mansucript. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Data_sets_for_The_influence_of_geochemical_variation_among_Glo...
 
Title Data sets for 'The influence of geochemical variation among Globigerinoides ruber individuals on paleoceanographic reconstructions' 
Description This dataset contains geochemical and morphological data for the planktic foraminifera Globigerinoides ruber. Descriptions of data can be found in the ReadME file and in the realted mansucript. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Data_sets_for_The_influence_of_geochemical_variation_among_Glo...
 
Title Integral projection model results of the planktonic foraminifer Trilobatus sacculifer 
Description Developmental plasticity, where traits change state in response to environmental cues, is well-studied in modern populations. It is also suspected to play a role in macroevolutionary dynamics, but due to a lack of long-term records the frequency of plasticity-led evolution in deep time remains unknown. Populations are dynamic entities, yet their representation in the fossil record is a static snapshot of often isolated individuals. Here, we apply for the first time contemporary integral projection models (IPMs) to fossil data to link individual development with expected population variation. IPMs describe the effects of individual growth in discrete steps on long-term population dynamics. We parameterize the models using modern and fossil data of the planktonic foraminifer Trilobatus sacculifer. Foraminifera grow by adding chambers in discrete stages and die at reproduction, making them excellent case studies for IPMs. Our results predict that somatic growth rates have almost twice as much influence on population dynamics than survival and more than eight times more influence than reproduction, suggesting that selection would primarily target somatic growth as the major determinant of fitness. As numerous palaeobiological systems record growth rate increments in single genetic individuals, and imaging technologies are increasingly available, our results open up the possibility of evidence-based inference of developmental plasticity spanning macroevolutionary dynamics. Given the centrality of ecology in palaeobiological thinking, our model is one approach to help bridge eco-evolutionary scales while directing attention towards the most relevant life-history traits to measure. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.t1g1jwt53
 
Description Turing Institute 
Organisation Alan Turing Institute
Country United Kingdom 
Sector Academic/University 
PI Contribution We have initiated conversations with the Turing Institute's Data Science for science and the humanities https://www.turing.ac.uk/research/research-programmes/data-science-science-and-humanities, with joint research meetings scheduled through March - May 2022 with a focus around Automated Phenotyping. The initial points of contact are Scott Hosking and Sebastian Ahnert, with a view to using our image bank to further catalyse software tools to extract phenotypes from computed tomography, and with a view of better understand genotypic-phenotypic flexibility. PhD Student James Mulqueeney has led further discussions in 22/23, and applied for a Turing Placement to formalise his knowledge of Artificial Intelligence and Machine Learning
Collaborator Contribution expertise, intellectual input and access to collaborative environment of like-minded researchers
Impact Too early
Start Year 2022
 
Title R Code (.Rmd) for 'The influence of geochemical variation among Globigerinoides ruber individuals on paleoceanographic reconstructions' 
Description This code runs through all the analysis discussed in 'The influence of geochemical variation among Globigerinoides ruber individuals on paleoceanographic reconstructions' whilst reproducing all supplementary figures and tables. For this code to run you will need the trace element, morphological and stable isotope data linked to this manuscript (10.6084/m9.figshare.21071203). 
Type Of Technology Software 
Year Produced 2023 
Open Source License? Yes  
URL https://figshare.com/articles/software/R_Code_Rmd_for_The_influence_of_geochemical_variation_among_G...
 
Title R Code (.Rmd) for 'The influence of geochemical variation among Globigerinoides ruber individuals on paleoceanographic reconstructions' 
Description This code runs through all the analysis discussed in 'The influence of geochemical variation among Globigerinoides ruber individuals on paleoceanographic reconstructions' whilst reproducing all supplementary figures and tables. For this code to run you will need the trace element, morphological and stable isotope data linked to this manuscript (10.6084/m9.figshare.21071203). 
Type Of Technology Software 
Year Produced 2023 
Open Source License? Yes  
URL https://figshare.com/articles/software/R_Code_Rmd_for_The_influence_of_geochemical_variation_among_G...