Insect relationships and evolution in deep time

Lead Research Organisation: University of Manchester
Department Name: Earth Atmospheric and Env Sciences

Abstract

Insects are the most diverse animal group: there are more than one million described species, which are key contributors to ecosystems on land. This makes the insects very important, but uncertainty remains regarding their origins and evolution. For example, how did their wings evolve, and from what? Over what timescale did their diversification take place? What makes them so successful? Limited knowledge on these, and other key questions, results from uncertain evolutionary relationships within the insects, especially amongst fossil groups which provide direct insights into the group's evolution. Analyses using the DNA of extant species are starting to resolve relationships between living orders, but the important early branching events in insect history remain problematic. This is because there are no testable, insect-wide analyses that place extinct orders - or extinct species likely to belong to living orders - on the insect tree of life. We propose a study that does just this, using established, computer-based approaches. It will include fossils from all extinct orders, and a range of other fossil species, which will be complemented by modern species and their DNA data. The project will be carried out at the University of Manchester by an interdisciplinary team and will allow us to create the first evolutionary tree of all insect orders, both living and dead. This will allow us to better understand the origin of insect wings; branching events early in insect evolution (i.e. how insects are related to each other at the deepest level); whether periods when the insects became more diverse very quickly are linked to evolutionary novelties or ecological developments; and the dynamics of major evolutionary changes. Improved clarity in insect relationships will result, and will be key to long-term research surrounding evolutionary processes, and the factors behind the group's success. This is a timely and multidisciplinary piece of work which will have international impact. The project will also provide the opportunity to engage the public, improving knowledge of both the insects, and of evolution itself.

Planned Impact

This project will have a range of beneficiaries in terms of economic and societal impacts. Palaeontology is a key subject for building enthusiasm and interest in science through public engagement - for example, DinoZone at the 2015 Cheltenham Science Festival, organised and staffed by the University of Manchester's palaeontologists, attracted 13,755 public attendees over the course of a week in 2015. The wider public are hence key beneficiaries of this project. In particular, the results - whose dissemination will be achieved through the pathways to impact - will be a very valuable tool for increasing public awareness of the importance of both fossils and insects. A focus of this outreach will be will be conveying the importance of palaeontology for understanding current pressures on ecosystems, the insects' key role in land-based ecosystems, and the contribution of wild insects to ecological services. This will in itself be highly beneficial, enabling education, and allowing members of the public to act as informed citizens, whilst inspiring a new generation of researchers. Furthermore, it will have direct impact on the support for conservation and study programmes. A clearer understanding in the public of the importance of the UK's fossil heritage, and role of insects in the UK economy will aid policy-makers through this increased support, and aid the government / government agencies and regulators when enforcing conservation programs (and in other conservation settings, e.g. tinyurl.com/mn65wht). That the results will have significant implications for our understanding of the history of the insects and the timing of their terrestrialisation, impacts on the public sector: numerous UK museums and galleries already display fossil insects (e.g. Natural History Museum, London; National Museums of Scotland), and the results of this project will inform these displays; many of these were collected in the Victorian Era, and it will demonstrate to the public that this rich cultural history of palaeontological investigation continues to this day. The proposed Summer of Science stand and its subsequent use within the museum sector for events such as the EU-wide Science Uncovered, and in Manchester Museum events will also impact on the museum sector. The PDRA staff working on this project will develop a wide-ranging skillset in phylogenetic methods, and a significant depth of knowledge of the insects, their evolutionary relationships, and their fossil record. Both skillsets will be directly beneficial for careers in palaeontology, evolutionary biology, or the heritage sector, and the outreach activities will prepare them equally well for a career within science communication. These impacts will occur within the three years of the project's course due to the continued efforts in two-way outreach events such as the proposed Summer of Science stand, and a regular blog on an already-popular and highly visible website (palaeontologyonline.com).

Publications

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Furness EN (2021) Evolutionary simulations clarify and reconcile biodiversity-disturbance models. in Proceedings. Biological sciences

 
Description We now have a completed phylogeny for the insects, which was a key aim of the award, which is close to submission and places all major fossils groups within the insect tree.
Exploitation Route Once published, this can be reused in a wide variety of settings to understand insect evolution
Sectors Other

 
Description This grant was in part used to support the following publication: Davies, N.S., Garwood, R.J., McMahon, W.J., Schneider, J.W. and Shillito, A.P., 2021. The largest arthropod in Earth history: insights from newly discovered Arthropleura remains (Serpukhovian Stainmore Formation, Northumberland, England). Journal of the Geological Society. This received widespred press coverage - it has an altmetric of 2074, and is placed in the 99th percentile of all outputs ever tracked - in fact, it's #2,969 of 20,443,577 outputs tracked by altmetric to date. The specimen related to this paper is now on display in the Sedwick Museum, Cambridge.
First Year Of Impact 2021
Sector Education,Culture, Heritage, Museums and Collections
Impact Types Cultural

 
Title Data from: Fossils improve phylogenetic analyses of morphological characters 
Description Fossils provide our only direct window into evolutionary events in the distant past. Incorporating them into phylogenetic hypotheses of living clades can help time-calibrate divergences, as well as elucidate macroevolutionary dynamics. However, the effect fossils have on phylogenetic reconstruction from morphology remains controversial. The consequences of explicitly incorporating the stratigraphic ages of fossils using tip-dated inference are also unclear. Here we use simulations to evaluate the performance of inference methods across different levels of fossil sampling and missing data. Our results show that fossil taxa improve phylogenetic analysis of morphological datasets, even when highly fragmentary. Irrespective of inference method, fossils improve the accuracy of phylogenies and increase the number of resolved nodes. They also induce the collapse of ancient and highly uncertain relationships that tend to be incorrectly resolved when sampling only extant taxa. Furthermore, tip-dated analyses under the fossilized birth-death process outperform undated methods of inference, demonstrating that the stratigraphic ages of fossils contain vital phylogenetic information. Fossils help to extract true phylogenetic signals from morphology, an effect that is mediated by both their distinctive morphology and their temporal information, and their incorporation in total-evidence phylogenetics is necessary to faithfully reconstruct evolutionary history. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.4xgxd2585
 
Title palaeoware/revosim: REvoSim and EnviroGen v3.0.0 
Description This is the public release of a new version of the REvoSim software with major updates, alongside minor improvements to the EnviroGen utility package. The model, and initial release was been described in detail in the following paper: Garwood, R.J., Spencer A.R.T. and Sutton, M.D., 2019. REvoSim: Organism-level simulation of macro- and microevolution. Palaeontology 62(3),339-355. https://doi.org/10.1111/pala.12420 Additions in this release are described in the following paper: Furness, E.N., Garwood, R.J. and Sutton, M.D., 2023. REvoSim v3.0.0: A fast evolutionary simulation tool with ecological processes. JOSS. Submitted. The code is archived on zenodo.org: 10.5281/zenodo.2531610. Other relevant references: Furness E.N., Garwood R.J., Mannion P.D. & Sutton M.D. 2021. Evolutionary simulations clarify and reconcile biodiversity-disturbance models. Proceedings of the Royal Society B 288(1949):20210240. https://doi.org/10.1098/rspb.2021.0240 Furness, E.N., Garwood, R.J., Mannion, P. D. & Sutton, M.D. 2021. Productivity, niche availability, species richness and extinction risk: Untangling relationships using individual-based simulations. Ecology and Evolution 11(13): 8923-8940. https://doi.org/10.1002/ece3.7730 Documentation: REvoSim Online Documentation EnviroGen Online Documentation Change log: The following has been changed since the last release. All additions are fully outlined in the documentation. REvoSim Systems. REvoSim processes (e.g. fitness, mutation, breeding, species ID) have been placed into structures called systems, which can be applied to user-defined portions of organism genomes. New genome architecture. Organisms now comprise a configurable number of 32-bit genome "words"- organisms, and different word combinations can be utilised by REvoSim's different systems. Pathogens. There is now a mechanism by which pathogens can be applied, killing individuals within the simulation. These can either drift, or evolve towards virulence. Masks for variables. A mechanism by which images can be used to spatially control the variables within a simulation has been added. Ecology added. Inter-organism interactions are now possible within the software. These are achieved through two mechanisms, and can alter organism fitness, or result in the transfer of energy between individuals. Additional seeding options. Associated with ecology, simulations can now be seeded with three or five species, known to form a food-chain in some interactions settings, and a trophic level is calculated for individuals. Logging. The software logging system has been rewritten for increased versatility - for the running log the software now allows a user to define a header, grid-level statistics, species level statistics which are output at polling iterations. Species ID. The species identification algorithm has been recoded to improve performance. Breeding. Organism breeding modes now include obligate as well as facultative sexual reproduction, asexual reproduction, and variable. In the latter a portion of the organism genome defines the probability of breeding sexually v.s asexually, allowing the level of recombination to evolve. Mutation. Similar to the variable breeding option, there is now a variable mutation mode in which mutation rate is under control of the genome and so can evolve. Random numbers. The random number system has been updated to employ the QRandomGenerator Class. Command line. REvoSim can now be launched from the command line, all options can be modified at launch, and runs initiated. Tests. Software tests have been added, and can outputs can be inspected by the user. EnviroGen Random numbers. The random number system has been updated to employ the QRandomGenerator Class. Fixed numerous bugs. Release information: Windows A zip containing all required binaries can be downloaded from the assets below. Alternatively an installer is provided. See notes below: Note 1: The .zip archive contains all REvoSim programs (REvoSim and EnviroGen). The .zip can be extracted and the programs run by double clicking the .exe files. All the required libraries have been included. Note 2: The windows installer will not overwrite any pre-existing REvoSim installations. Mac A zip containing the REvoSim programs (REvoSim and EnviroGen) as DMGs can be downloaded from the assets below. The software can be run by double clicking on either. To install the software, drag and drop the required DMGs into the Applications folder. In both these cases you may be required to the approve the software in security and privacy settings before it will launch. Note 1: Builds are x86-64, and so the software will not run at optimal speed on the new apple silicon Macs (tests suggest the speed is acceptable, however). Linux Any Linux users requiring a Linux build should contact palaeoware@gmail.com. 
Type Of Technology Software 
Year Produced 2023 
Impact This allows a wider simulation of evolution and will allow ecological interactions within the software - there are 3 papers about to be submitted using the new tools 
URL https://zenodo.org/record/7699771
 
Title palaeoware/trevosim: TREvoSim v1.0.0 
Description This is the first public release of the TREvoSim software. This release and the underlying model has been described in detail in the following paper: Keating, J.N., Sansom, R.S., Sutton, M.D., Knight, C.G., and Garwood, R.J. 2020. Morphological phylogenetics evaluated using novel evolutionary simulations. Systematic Biology. The code is archived on zenodo.org. Documentation: TREvoSim Online Documentation Change log: Initial public release. Release information: Windows A zip containing all required binaries can be downloaded from the assets below. Alternatively an installer is provided. See notes below: Note 1: The .zip archive contains an executable TREvoSim.exe. The .zip can be extracted and the program run by double clicking this.exe file in the ./bin folder. All the required libraries have been included and are found in the ./bin folder. Mac A zip containing TREovSim can be downloaded from the assets below. To install the software, drag and drop the required .app folder(s) into the Applications folder. You may be required to the approve the software in security and privacy settings before it will launch. Linux Any Linux users willing to test a Linux build should contact palaeoware@gmail.com. 
Type Of Technology Software 
Year Produced 2020 
Open Source License? Yes  
Impact Work for the 2020 preprint associated with this grant in its first year has resulted in the development of a new version of this software accompanying that paper. This allows the simulation of more realistic morphological phylogenetic data, ultimately allowing that preprint to demonstrate that adding fossils to phylogenies is beneficial. 
URL https://zenodo.org/record/3619355
 
Title palaeoware/trevosim: TREvoSim v2.0.0 
Description This is the release of a new version (v2.0.0) of TREvoSim. The first release and the underlying model was described in detail in the following paper: Keating, J.N., Sansom, R.S., Sutton, M.D., Knight, C.G. & Garwood, R.J. 2020. Morphological phylogenetics evaluated using novel evolutionary simulations. Systematic Biology 69(5): 897-912. doi:10.1093/sysbio/syaa012 Version 2.0.0 accompanies the preprint and paper below: Mongiardino Koch, N., Garwood, R.J. & Parry, L.A. Preprint. Fossils improve phylogenetic analyses of morphological characters. bioRxiv. doi: 10.1101/2020.12.03.410068v1 Mongiardino Koch, N., Garwood, R.J. & Parry, L.A. 2021. Fossils improve phylogenetic analyses of morphological characters. Proceedings of the Royal Society B: Biological Sciences The code is archived on zenodo.org: Documentation: TREvoSim Online Documentation Change log: The changes in v2.0.0 are described and discussed fully in the associated paper. In brief, these allow TREvoSim v2.0.0 trees and data to achieve benchmarks calculated from twelve total evidence analyses, as well as respresenting ongoing development of the package. Changes are: Addition of multiple playing fields option. Playing fields can have independent or identical environments. The option to overwrite a random individual when a juveniles is returned to the playing field (instead of the least fit one). User control of the fitness target in the fitness algorithm (see Keating et al. 2020). A fitness histogram functionality to assess the fitness landscape in the simulation. User control of the strength of selection (see Mongiardino Koch et al. 2021 for discussion). Multiple environments per playing field. Organism fitness is assessed against each environment, and the fitness of an organism is defined by the environment they are best suited to. The code has been refactored (the biggest change being to the underlying data structures/classes), and the simulation now uses Qt QRandomGenerator tools rather than incorporating random data. A user-accessible test suite has been added. Release information: Windows A zip containing all required binaries can be downloaded from the assets below. Alternatively an installer is provided. See notes below: Note 1: The .zip archive contains an executable TREvoSim_2.0.0.exe. The .zip can be extracted and the program run by double clicking this.exe file in the ./bin folder. All the required libraries have been included and are found in the ./bin folder. Mac A zip containing TREovSim can be downloaded from the assets below. To install the software, drag and drop the required .app folder(s) into the Applications folder. You may be required to the approve the software in security and privacy settings before it will launch. Linux Any Linux users willing to test a Linux build should contact palaeoware@gmail.com. 
Type Of Technology Software 
Year Produced 2021 
Impact preprint then paper (Mongiardino Koch, N., Garwood, R.J. and Parry, L.A., 2021. Fossils improve phylogenetic analyses of morphological characters. Proceedings of the Royal Society B, 288(1950), p.20210044.) demonstrating that fossils improve phylogenetic analyses of morphological characters - a key plank of this project, but important also for palaeontologists, phylogeneticists and zooloigsts. 
URL https://zenodo.org/record/4564524