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An individual-based perspective on macroevolution

Lead Research Organisation: University of Southampton
Department Name: National Oceanography Centre Southampton

Abstract

Consider the weights of the 1500 or so commuters onboard the 07:52 Esher to London Waterloo train service. Weight has many health implications, affecting both life expectancy and reproductive potential. The 18 stone man opposite might not seem an ideal catch for a physically-fit impressionable type if she considers only his weight. If, however, she also sees he is 6 and a half feet tall with an athletic appearance (perhaps he plays rugby), then he becomes a much more attractive proposition.

Biologists often attempt to understand the evolution of traits like height and weight on their own. It is not individual traits that survive, reproduce and die though, but whole individuals. If the individuals of a species are successful, then the species will be too. The connection highlights the link between the traits that define species, evolution within species and the formation of new species is a key part of evolutionary biology, but one for which lots of data are rare. To understand it, we need to study competition among species in different environments. We also need to sample individuals in populations over and over again to see how these pressures change over time.

Only the fossil record can give direct evidence of historical groups of species and how they have changed over vast periods of time. The exceptional preservation of fossilised planktonic foraminifera - single-celled, sexual organisms living in all of the world's oceans - means it is possible to home in on abrupt or gradual climate change, seeing which groups succeed and, importantly, which groups fail: competition and climate change have very different impacts on the generation of new species and the extinction of living ones. The enviable preservation of whole foraminifera as fossils mean I can sample their fossil record in the same way as scientists sample laboratory experiments to see what drives evolution. In doing so, I will be the first to use real data to test key assumptions on how variation among individuals affects variation among species.

Understanding evolution is a fundamental concern, especially in a world characterised by rapid responses to human-induced threats. While there have recently been many theoretical advances in how small-scale trends might map to large-scale diversity patterns, evidence from real data is still largely missing. Macroperforate planktonic foraminifera have survived and adapted to ongoing climate change and rapid global warming before. In each instance, assemblages were much altered after the event as new species rose to dominate their biodiversity. Results spanning local to global scales, from the deep past to the present day, will not only provide new insight into how biodiversity arrived at its current state, but will also lead to new work that improves predictions of its prospects in the future.

Planned Impact

In addition to the academic and commercial beneficiaries, my proposal has great potential to reach out to the general public because changes in individuals and species can clearly be seen in fossil communities. To engage the wider public, I will use established resources in the press offices of the University of Bristol and NERC and also propose to extend my program of existing workshops and public lectures on "Mathematics in the Real World". In addition, I propose to launch a new project in Einstein's Garden at the Green Man Festival. This interactive workshop will give festival goers the chance to contribute to an animated film based on the evolution of planktonic foraminifera, and will be planned and executed in collaboration with a science communicator I currently work with and an independent film-maker. The great strength of an empirical approach is the opportunity for participants (school children, festival-goers, and potentially many more) to see with their own eyes the evolution of different types of species as climate change gives them particular advantages and disadvantages relative to their competitors.

Publications

10 25 50
 
Description I have built a growing team of PDRAs, Research Technicians and PhD students working towards the goals of my NERC Advanced Fellowship. Over the last year, my Fellowship and Wellcome Trust New Investigator Award have both ended and my new NERC Large Grant has begun. I continue to grow my funding portfolio as Co-Investigator on a NERC/BBSRC award questioning the role of plasticity during domestication that began in January 2019 (PI Chapman, Biological Sciences, University of Southampton). My lab now consists of 3 PDRAs, 3 PhD students and 2 RAs, which is the target size I set out as a goal during my Fellowship interview.

My work continues to develop an independent research base, amalgamating existing or collating new data. I have been Communicating Editor on a special issue of Philosophical Transactions of the Royal Society - Series B focusing on aspects of my Advanced Fellowship and continue to be invited to international workshops convened by international research leaders, emphasising my established position as an independent researcher. The NERC Large Grant is a new collaboration across the Universities of Southampton, Bristol, Leeds and University College London. I lead this £3.2m FEC PISTON project NE/P019269/1, which consolidates all facets of my multidisciplinary career path to address an outstanding question in 21st century evolutionary ecology. My NERC Advanced Fellowship provided me the platform and intellectual breathing space to develop such an ambitious proposal. I am immensely grateful for the opportunity and excited to start publishing our results and methodological innovations. The NERC/BBSRC Award develops related questions on the role of plasticity during adaptive divergence, but does so from an explicitly transcriptomic perspective on a very different study system (Brassicas) to PISTON. I continue to believe that the best approach is to be question driven in my research rather than system specific.

I am also collaborating increasingly frequently with international researchers at UC Berkeley, Trinity College Dublin and other world-leading institutions. My profile is raised further through contributions to learned societies - I was elected Honorary Treasurer of the British Ecological Society in 2017 and am a member of the Core Committee of the COMPADRE/COMADRE project on data-driven comparative demography. I joined the journal Evolution as an Associate Editor in January 2019.

Our data compilation efforts continue to grow, with a series of publications in revision, in review or in press. My team generated the largest database of microevolutionary morphological change to over 30,000 individuals with spatial replication, in addition to the largest temporal record from a single site (10,200 individuals in one species), and have formed a new collaboration with the Natural History Museum to digitise a 15,000 strong Buckley Collection of planktonic foraminifera (http://jm.lyellcollection.org/content/early/2016/12/15/jmpaleo2016-020). My commitment to this evidence base being openly available is clear from my increasing prominence on figshare, sharing the data or simulation code used to generate my outputs (http://figshare.com/authors/Thomas%20Ezard/431400), all computer code on my first author publications and data visualisation apps http://pyramids.cpc.ac.uk/ to allow end-users to explore the data that underpins my research

I continue to prioritise world-class outputs, in field-leading journals such as Nature Ecology and Evolution, Ecology Letters and American Naturalist, as well as interdisciplinary outlets such as Nature Communications and PNAS. I continue to prioritise a diversified research portfolio, building on the funded science outlined above to ensure resilient foundations for my changing research career. These outputs should be taken forward by a diverse range of academics, from evolutionary biologists to palaeoclimatologists and engineers. While the speciation components of this Fellowship are being delivered within NE/P019269/1, the extinction aspects continue to be developed through related PhD projects funded through University of Southampton's Institute for Life Sciences (Lorna Kearns) and the INSPIRE Doctoral Training Program (Chloe Todd) as I build pilot data sets towards future grant submissions.
Exploitation Route Automated dating of geological deposits. Development of open-source automated algorithms for feature extraction in all aspects of the life and engineering sciences.
Sectors Environment

Healthcare

URL http://fusionecology.org/
 
Description Advanced Training Short Course
Amount £30,008 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 02/2017 
End 02/2017
 
Description FAPESP/UoS Partnership
Amount £20,000 (GBP)
Organisation São Paulo Research Foundation (FAPESP) 
Sector Public
Country Brazil
Start 03/2014 
End 03/2016
 
Description NERC Large Grant
Amount £3,200,493 (GBP)
Funding ID NE/P019269/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2017 
End 10/2022
 
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 12/2022
 
Description Wellcome Trust New Investigator
Amount £228,603 (GBP)
Funding ID WT103780AIA 
Organisation Wellcome Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 09/2014 
End 10/2017
 
Title Dataset accessibility statements and R code (pdf & knitr Rnw) to run analyses for Ezard & Purvis (2016) Ecology Letters 19: 899-906. https://doi.org/10.1111/ele.12626 
Description Dataset accessibility statements and R code (pdf & knitr Rnw) to run analyses for Ezard & Purvis (2016) Ecology Letters 19: 899-906. https://doi.org/10.1111/ele.12626 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Dataset_accessibility_statements_and_R_code_pdf_knitr_Rnw_to_r...
 
Title Dataset accessibility statements and R code to run analyses for Ezard & Purvis (2016) Ecology Letters 19: 899-906. https://doi.org/10.1111/ele.12626 
Description Dataset accessibility statements and R code (pdf & knitr Rnw) to run analyses for Ezard & Purvis (2016) Ecology Letters 19: 899-906. https://doi.org/10.1111/ele.12626 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Dataset_accessibility_statements_and_R_code_pdf_knitr_Rnw_to_r...
 
Title Dataset accessibility statements and R code to run analyses for Ezard & Purvis (2016) Ecology Letters 19: 899-906. https://doi.org/10.1111/ele.12626 
Description Dataset accessibility statements and R code (pdf & knitr Rnw) to run analyses for Ezard & Purvis (2016) Ecology Letters 19: 899-906. https://doi.org/10.1111/ele.12626 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/Dataset_accessibility_statements_and_R_code_pdf_knitr_Rnw_to_r...
 
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
 
Title Size and shape data of Globigerinoidesella fistulosa, Trilobatus sacculifer and intermediate specimens from ODP Site 1115 
Description Planktonic foraminifera are extremely well-suited to study evolutionary processes in the fossil record due to their high-resolution deposits and global distribution. Species are typically conservative in their shell morphology with the same geometric shapes appearing repeatedly through iterative evolution, but the mechanisms behind the architectural limits on foraminiferal shell shape are still not well understood. To understand when and how these developmental constraints can be overcome, we study morphological change leading up to the origination of the unusually ornate species Globigerinoidesella fistulosa. Our results show that the origination of G. fistulosa from the Trilobatus sacculifer plexus involved an amalgamation of three different heterochronic expressions: addition of chambers (hypermorphosis), earlier onset of protuberances (pre-displacement), and steeper allometric slope (acceleration) as compared to its ancestor. We argue that the protuberances unique to G. fistulosa were necessary to sustain a surface-area: volume ratio that could host sufficient numbers of photosymbionts. Our work provides a case study of the complex combination of processes required to produce unusual shell shapes and highlights the importance of developmental processes in evolutionary origination. 
Type Of Material Database/Collection of data 
Year Produced 2023 
Provided To Others? Yes  
URL https://datadryad.org/stash/dataset/doi:10.5061/dryad.3bk3j9kqh
 
Description FAPESP/UoS Partnership Award 
Organisation Federal University of Sao Carlos
Country Brazil 
Sector Academic/University 
PI Contribution This was a partnership award to establish a new collaboration between Dr Tiago Quental (USP) and Dr Thomas Ezard (U. Southampton). As part of the project, we successfully pitched a theme issue on "The Regulators of Biodiversity in Deep Time" to Philosophical Transactions of the Royal Society, which was published in 2016 under the editorship of Ezard (Communicating Editor), Quental and Professor Mike Benton (University of Bristol). My contributions were intellectual development of the project, corresponding author on our manuscript, co-ordination of workshops in Southampton (including raising of additional funds to support early career attendance), acting as Communicating Editor for the special issue, which strengthens my position at the forefront of my field.
Collaborator Contribution Intellectual development of the project, co-ordination of workshops in Sao Paolo (including raising of additional funds to support early career attendance) and acting as Editor for the special issue and writing manuscripts.
Impact Special issue of Phil Trans Roy Soc B appeared in 2016, including our co-authored review of the state of the field: http://rstb.royalsocietypublishing.org/content/371/1691/20150216
Start Year 2014
 
Title 3DKWMI 
Description The rapid and repeatable characterization of individual morphology has advanced automated taxonomic classification. The most direct study of evolutionary processes is, however, not from taxonomic description, but rather of the evolution of the traits that comprise individuals and define species. Repeatable signatures of individual morphology are crucial for analysing the response to selection at scale, and thus tracking evolutionary trajectories through time and across species boundaries. 3DKMI is an open-source MATLAB package designed for the study of morphology using three-dimensional (3D) Krawtchouk moment invariants. The volumetric features derived from the 3D images remain stable under translation, scaling and rotation and, for an image of size 128 × 128 × 128 can be computed in less than 0.1 s. We applied our package as a case study on a collection of 300 X-ray computed tomography scans of planktonic foraminifera specimens across five species to assess the invariance of the features under different transformations. 
Type Of Technology Webtool/Application 
Year Produced 2024 
Open Source License? Yes  
Impact Too soon to tell 
URL https://besjournals.onlinelibrary.wiley.com/doi/10.1111/2041-210X.14388
 
Title foram3D: an R package for automated trait measurements from CT scans 
Description an open-source R package to analyse growth in three-dimensional space. Using only the centroid xyz coordinates of every chamber, the functions determine the growth sequence and check that chambers are in the correct order. Once the order of growth has been verified, the functions calculate distances and angles between subsequent chambers, determine the total number of whorls and the number of chambers in the final whorl at the time each chamber was built, and, for the first time, quantify trochospirality. The applications of this package will enable repeatable analysis of large data sets and quantification of key taxonomic traits. 
Type Of Technology Webtool/Application 
Year Produced 2023 
Open Source License? Yes  
Impact Already being cited and used on more general work beyond foraminifera 
URL https://jm.copernicus.org/articles/41/149/2022/
 
Description Bright Club Guildford Christmas Special 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Research-based stand-up comedy.

Bright Club is an evening of research-based stand-up comedy sets, performed by academics to the general public. 165 tickets were sold for the christmas special, which was filmed and the video is on YouTube. My set consists of a retelling of my American Na
Year(s) Of Engagement Activity 2012
 
Description Bright Club Winchester Science Festival 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Stand up comedy set based on my academic work

N/A
Year(s) Of Engagement Activity 2014
URL https://www.facebook.com/events/720202108003064/?ref=22
 
Description Career Spotlight: Anieke Brombacher 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Interview myth-busting research activities during research cruises on the Joides Resolution research vessel.
Year(s) Of Engagement Activity 2019
URL https://joidesresolution.org/career-spotlight-micropaleontologist-anieke-brombacher/
 
Description Finding fossils (biostratigraphy based engagement tasks) 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact Demystify how biostratigraphy works in an interactive and educational setting.
Year(s) Of Engagement Activity 2019
URL https://joidesresolution.org/finding-fossils-a-biostratigraphy-activity/
 
Description Mathematics in the Life Sciences 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact Presentation to A-Level students on the benefits of mathematics in the life sciences, and how we use models as experiments to learn more about the complexity of the natural world.
Year(s) Of Engagement Activity 2016
 
Description Primary school workshop on mathematics in evolution. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Primary school workshop on mathematics in evolution.
Year(s) Of Engagement Activity 2016
 
Description Protecting Our Planet (POP) Day 2024 Mathematics Panel 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Schools
Results and Impact Presentation of AI pipelines as a route to extract evolutionarily relevant trait data.
Year(s) Of Engagement Activity 2024