The role of trade-offs in the evolution of senescence

Lead Research Organisation: University of Sheffield
Department Name: Animal and Plant Sciences

Abstract

Spoiler alert: we are all going to die! Death is certain in all organisms: from bacteria, to us humans, and to the millenarian Bristlecone pines. However, the driving question in ageing research is not so much the end point, death, but rather what happens to our bodies before we reach that destination. Specifically, why do we become more fragile and decrepit prior to death? This increase in mortality risk and decline in fertility with age, known as senescence, has a strong influence on our lifetime agenda: the age at which we graduate from school, are expected to get married and have babies, get a permanent job and retire from it, to mention just a few. All of these are critical events in our lives that are established by governments using, among others, estimates of senescence rates of each country's human populations. When senescence is a bit slower, as in Northern European countries, and governments start to contemplate the idea of reducing the number of work hours per week while postponing the age at retirement, as it is currently being hotly debated in Germany and Denmark.

Get ready to be jealous: it turns out that senescence is not universal! Some animals and plants out there do not experience it. Yet, since the early inception of ageing research, the main theories to explain the occurrence of senescence have treated senescence itself as unavoidable and unescapable. My colleagues and I have recently disproved this fundamental tenet of life history theory in a publication in Nature. We have shown that, in fact, most plants and many animal species do not become more decrepit as they age. This finding drastically reshapes the direction that ageing research has taken historically. It is indeed a particularly exciting time to partake in ageing research because our finding has provoked a paradigm shift, forcing ageing research to move on from the question "Why do we senesce?" towards "Why and how do some species senesce but others do not?".

Do you wish to understand why we humans age? How about stepping away for a bit and examining how other species manage to escape senescence? My research will examine the mechanisms by which animal and plant species senesce or escape senescence. I will determine the aspects of a species' anatomy, physiology, habitat and evolutionary history that make it more or less vulnerable to ageing. To do so, I will examine the roles of physiological and macro-evolutionary trade-offs in the evolution or escape of senescence across the tree of life examining senescence trajectories in over 2000 animal and plant species from a database that I have developed in the last decade, and a set of long-term demographic datasets of species with complex life histories such as carnivorous plants or orchids with the ability of long-term dormancy (like a bear). Findings from this research are likely to pinpoint the habitats, abiotic conditions and features of taxonomic groups that allow species to operate at high performance levels for longer.

Planned Impact

In addition to the academic and commercial beneficiaries outlined below, my project has a great potential to appeal the general public. Just as many researchers have believed until very recently that ageing is inevitable, so did the general public. The communication through outreach activities that this is not the case is a primary point of outreach agenda. To engage with the general public, I will use the resources of the University of Sheffield and NERC to extend my research findings into the public's knowledge arena. I will also work with the Botanical Garden of Sheffield to organized sessions where children and adults will be informed on the various mechanisms by which plants can slow down ageing, while presenting them with some of the longest-lived records hosted in the greenhouses. In addition, I will continue with my active blogging activities and tweets on science matters.

As I did during my time in the USA, where I served as chair of the ESA Student Section and secretary of the Plant Population Ecology Section, I will take proactive steps towards engaging with the University of Sheffield early-career researchers, and with those of the British Ecological Society. Carrying out this task is something that will come natural to me, as I am one of the founders of the International Network of Next-Generation Ecologists (www.innge.net). I will use my past experiences with the ESA to work with the BES to create an early-career section that will secure continuity in economic and mentoring support of recently-graduated ecologists in the "limbo" postdoctoral/fellow stages.
 
Description The two axes framework that I published in PNAS in 2016 as first author has important ramification for the classification of plant species' ability to undergo or escape from senescence, as highlighted in my recent publication in New Phytologist. This framework has allowed me to explore how species' tradeoffs between survival and reproduction render them more likely to undergo or escape from senescence (New Phytologist 2017), and how the turnover of ramets within clonal plants also undergo strong rates of senescence (Evolutionary Ecology 2017). A recent publication in PLOS One with colleagues has highlighted a promising framework to understand the variability in ageing trajectories that I described in a Nature publication in 2014.
Exploitation Route Applicability of ranks of species' ability to escape from senescence may now be linked, through my own work in New Phytologist 2017, to functional traits such as SLA. This work could be expanded by functional ecologists to take shortcuts in the management of senescent species. My recent publication in Ecology Letters 2018 also shows the usefulness of this framework to examine the vulnerability of species' population dynamics to predicted changes in climatic regimes.
Sectors Creative Economy,Healthcare

URL https://compadredb.wordpress.com
 
Description A global open-access repository of plant and animal demographic data
Amount $604,923 (USD)
Organisation National Science Foundation (NSF) 
Sector Public
Country United States
Start 09/2017 
End 08/2020
 
Description How will climate change and poaching affect endemic South African living rocks?
Amount £5,000 (GBP)
Organisation University of Oxford 
Sector Academic/University
Country United Kingdom
Start 03/2018 
End 12/2018
 
Description Practical utility of new classes of species distribution models
Amount $396,250 (AUD)
Organisation Australian Research Council 
Sector Public
Country Australia
Start 01/2018 
End 12/2020
 
Description sAPROPOS - Analysis of PROjections of POpulationS
Amount € 32,130 (EUR)
Organisation German Centre for Integrative Biodiversity Research 
Sector Charity/Non Profit
Country Germany
Start 10/2016 
End 12/2018
 
Title COMADRE database 
Description Database of matrix population models for animals 
Type Of Material Database/Collection of data 
Year Produced 2016 
Provided To Others? Yes  
Impact Elton Award of the BES to early career researcher 
URL http://www.comadre-db.org
 
Title MOSAIC trait database 
Description Database files for the MOSAIC database (See associated manuscript: MOSAIC: A Unified Trait Database to Complement Structured Population Models for more information and guidance). See, also, user guide and further information on the MOSAIC portal: https://mosaicdatabase.web.ox.ac.uk/ The primary key for linking databases is the species name. File #1 - Primary trait database file, organised by species name (csv). Filte #2 - ERA-5 climate data for all population models in COMADRE, COMPADRE, and PADRIN (csv). Organised by population model ID. File #3 - OTL phylogeny for species in the COMADRE and COMPADRE databases. Note that these data files are intended for loading and use in R using the ape package. (txt) 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/MOSAIC_trait_database/21035857
 
Title MOSAIC trait database 
Description Database files for the MOSAIC database (See associated manuscript: MOSAIC: A Unified Trait Database to Complement Structured Population Models for more information and guidance). See, also, user guide and further information on the MOSAIC portal: https://mosaicdatabase.web.ox.ac.uk/ The primary key for linking databases is the species name. File #1 - Primary trait database file, organised by species name (csv). Filte #2 - ERA-5 climate data for all population models in COMADRE, COMPADRE, and PADRIN (csv). Organised by population model ID. File #3 - OTL phylogeny for species in the COMADRE and COMPADRE databases. Note that these data files are intended for loading and use in R using the ape package. (txt) 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL https://figshare.com/articles/dataset/MOSAIC_trait_database/21035857/1
 
Title Transient amplification enhances the persistence of tropicalising coral assemblages in marginal high latitude environments 
Description Predicting the viability of species exposed to increasing climatic stress requires an appreciation for the mechanisms underpinning the success or failure of marginal populations. Rather than traditional metrics of long-term population performance, here we illustrate that short-term (i.e., transient) demographic characteristics, including measures of resistance, recovery, and compensation, are fundamental in the poleward range expansion of hard corals, facilitating the establishment of coral populations at higher latitudes. Through the annual census of tropical and subtropical Acropora spp. colonies in Japan between 2017-2019, we show how enhanced transient amplification (i.e., short-term increases in population growth following disturbance) supports the persistence of coral assemblages within more variable high-latitude environments. The transient dynamics of both the tropical and subtropical assemblages were strongly influenced by their corresponding recruitment patterns. However, we demonstrate that variation in colony survival and fragmentation patterns between the two assemblages determines their relative capacities for transient amplification. This latitudinal variation in the transient dynamics of Acropora spp. assemblages emphasises that coral populations can possess the demographic plasticity necessary for exploiting more variable, marginal conditions. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.d7wm37q43
 
Description sAPROPOS 
Organisation German Centre for Integrative Biodiversity Research
Country Germany 
Sector Charity/Non Profit 
PI Contribution Through the development of the demographic databases and demographic analyses performed in this grant, I have built a partnership with the German Centre for Biodiversity, iDiv, in Leipzig, to construct models that predict future performance of animal and plant populations worldwide. Partners include Prof Tiffany Knight and Prof Stan Harpole
Collaborator Contribution Prof Tiffany Knight has hired a postdoc on this project and a PhD students; both are co-supervised by me too and make frequent visits to my research group.
Impact Two papers are being written, and a new database, PADRINO, has originated: https://github.com/levisc8/Padrino.github.io
Start Year 2017
 
Title R-Age R library 
Description This R library allows for the calculation of various life history traits from matrix population models. It is aimed at interacting with any type of matrix population model, as well as with the demographic data stored in the COMPADRE and COMADRE databases. 
Type Of Technology Software 
Year Produced 2018 
Open Source License? Yes  
Impact I use this library to teach my students at Oxford, as well as at various weeklong workshops I have organised (e.g. Mexico in 2017, Sheffield in 2018) 
URL http://www.compadre-db.org
 
Title compadreDB R library 
Description An R library (under development) aimed at interacting with the COMPADRE and COMADRE open-access databases (www.compadre-db.org). Details and software can be found here: https://github.com/jonesor/compadreDB 
Type Of Technology Software 
Year Produced 2018 
Impact This package is used in many workshops that I run (e.g. Mexico in 2017, Sheffield in 2018) for students and postdocs interested in comparative demographics 
URL http://www.compadre-db.org
 
Description Advanced approaches to population modeling using Integral Projection Models 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact A 3-hour workshop teaching participants the parameterisation and implementation of integral projection models for ecological questions, organised at the EvoDemoS meeting at the University of Virginia, USA
Year(s) Of Engagement Activity 2016
 
Description All creatures fast and slow 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact I organised a three-day working group with research scholars and practitioners at the University of Oxford exploring ecological ramifications of the fast-slow continuum of life history theory
Year(s) Of Engagement Activity 2017
 
Description COMPADRE Plant Matrix Database & COMADRE Animal Matrix Database 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact I organised a 3-h workshop at the Evolutionary Demography Society annual meeting in Lyon, France, to teach participants how to harness the demographic information from www.compadre-db.org for comparative analyses
Year(s) Of Engagement Activity 2018
URL https://evodemo2018.sciencesconf.org
 
Description Comparative approaches in ecology and evolution 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact A workshop hosted at the Max Planck Institute for Demographic Research (Rostock, Germany) where my international co-instructors and I taught state-of-the-art techniques to bring together ecological and evolutionary questions using big data
Year(s) Of Engagement Activity 2016
 
Description Dispatches of Frontiers in Ecology and the Environment 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact My work on demographic databases and their role in conservation science and zoos was highlighted in the dispatches of the prestigious general-public publication Frontiers in Ecology and the Environment
Year(s) Of Engagement Activity 2017
URL http://onlinelibrary.wiley.com/doi/10.1002/fee.1453/epdf
 
Description Integral Projection Models: construction, analyses and interpretation 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact I organised a weeklong workshop to teach participants the implementation, analyses and interpretation of integral projection models in partnership with TransmittingScience, Barcelona, Spain
Year(s) Of Engagement Activity 2017
URL https://www.transmittingscience.org/courses/ecology/integral-projection-models-demography-continuous...
 
Description Integral Projection Models: construction, analyses and interpretation 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact A workshop organised with the partnership of TransmittingScience in Barcelona, Spain, to teach participants the construction, parameterisation and interpretation of integral projection models
Year(s) Of Engagement Activity 2016
URL https://www.transmittingscience.org/courses/ecology/integral-projection-models-demography-continuous...
 
Description International collaboration in ecology: why should I and how do I do It? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact I was invited to give a talk on how to carry out international collaborations, highlighting some of the challenges and opportunities that doing so has brought to my own academic career. This event took place at the annual meeting of the Ecological Society of America
Year(s) Of Engagement Activity 2017
URL https://eco.confex.com/eco/2017/webprogram/Session13096.html
 
Description Introduction to matrix population models and comparative population biology using the COM(P)ADRE Matrix Databases 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact I organised a 4-h workshop at the annual meeting of the Ecological Society of America to teach participant how to harness the analytical power of the COMPADRE and COMADRE open-access databases
Year(s) Of Engagement Activity 2017
URL https://eco.confex.com/eco/2017/webprogram/WORK.html
 
Description Introduction to population models and comparative demography 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact A three-day workshop teaching undergraduates, PhD students and postdocs at the University of Exeter tecniques to model population dynamics using matrix population models
Year(s) Of Engagement Activity 2016
 
Description Lightning talk session on Projection of Demographic Responses to Climate Change 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact I organised a lightning talk session showcasing the researcher carried out by 6 early career researchers in the working group "sAPROPOS" that I lead at the German Centre of Biodiversity iDiv, in Leipzig.
Year(s) Of Engagement Activity 2017
URL https://www.idiv.de/sdiv/working_groups/wg_pool/sapropos.html
 
Description Love Nature blog 
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 I was interviewed by a blogger on my research using large open-access demographic data. The blog was posted in the Love Nature blog
Year(s) Of Engagement Activity 2016
URL http://community.lovenature.com/blog/explore-the-incredible-work-of-computer-conservationists
 
Description Macro-ecology through the lens of comparative demography 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact A 2-h workshop organised at the annual meeting of the British Ecological Society where we taught participants intro-level skills to run comparative analyses using open-access, big demographic data
Year(s) Of Engagement Activity 2016
URL https://www.britishecologicalsociety.org/bes-annual-meeting-workshops/
 
Description Modelos de proyección integral y demografía comparada 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Undergraduate students
Results and Impact I organised a weeklong course at the UNAM (Mexico) in Spanish to teach undergraduate and postgraduate students various demographic analytical techniques
Year(s) Of Engagement Activity 2017
 
Description Stage-based demographic models in ecology, evolution and conservation biology 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact I organised a weeklong workshop teaching participants demographic techniques for ecology and evolution at the University of Sheffield. This workshop was hosted under the economic support of a NERC ATSC grant
Year(s) Of Engagement Activity 2018
URL https://robsalguero.wixsite.com/nercdemography
 
Description Webinar demography beyond the population 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact A webinar organised with selected authors of the special feature that I edited for the British Ecological Society "Demography beyond the population". In the webinar, authors provided a general-public explanation on the important of demography for urgent questions in ecology, evolution and conservation science
Year(s) Of Engagement Activity 2016
URL https://methodsblog.wordpress.com/2016/02/17/demography-beyond-the-population-webinar/
 
Description Webinar: A repertoire of the best research carried out by the Early Career Ecologist Section of the Ecological Society of America 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I organised a webinar highlighting the research by the winner and the runner-ups of the competition for the Award in Research Excellence I created for the Early Career Ecologist Section of the Ecological Society of America, where I was the chair in 2016-2017
Year(s) Of Engagement Activity 2017