Comparative venom transcriptomics of centipedes: evolutionary diversification of a key ecological adaptation

Lead Research Organisation: The Natural History Museum
Department Name: Life Sciences

Abstract

Although most lay people have little problem in identifying creatures like jellyfish, wasps, spiders, and scorpions as potentially dangerous venomous organisms, far fewer know that the ca. 3,300 species of centipedes possess potent venoms. A pair of strong venom claws is located just behind the head, and they house large venom glands that contain complex cocktails of venom components. Unfortunately we know almost nothing about the make-up of centipede venom, which leaves not only a large hole in our understanding of an ecologically important group, but it also compromises our general understanding of venom evolution in the animal kingdom. This study aims to remedy this ignorance by performing the first extensive and intensive analysis of the composition of centipede venoms. This project will take a genetic approach, and will characterize the toxin profiles from the venoms of five species of centipedes. These five species have been chosen to represent all major groups of centipedes. For each species, up to half a million mRNA sequences will be characterized. These precursor molecules are the templates for the production of toxin proteins. By comparing the profiles of these sequences across the selected species we can start to address important questions relating to the evolution of venoms and venomous organisms. The most basic question that can be answered is simply: what toxins are expressed in the venom glands of centipedes? The answer to this question will be the basis for answering the other questions. Does centipede venom have many toxins in common with the venoms of other groups? We already know from previous research that different groups of venomous animals can recruit many similar toxins into their venom. They do this by taking a gene coding for a normal body protein, duplicating it, and expressing one of the copies specifically in the venom gland. Changes in the sequence of the gene can create changes in the protein, and this can change the protein's function to be more effective as a toxin. Preliminary work, however, has suggested that centipede venom may contain many toxins not (yet?) found in other groups. This study will allow us to see how many venom components in centipedes are unique to them. Another major question that can be addressed with the new data is whether the diversification of the centipede species and their toxins went hand in hand. By integrating the family trees of the toxin genes and the centipedes we can infer whether particular episodes in the evolution of centipedes are associated with bouts of toxin evolution as well. We can also infer, by incorporating data from other venomous and non-venomous animals, from what kind of genes the toxin genes in centipedes have evolved. Since there were no centipede data available till now, we can broadly reassess our current understanding of the pattern of toxin in evolution across all animals. We can use the new data also to ask what kinds of processes were important in shaping the composition of centipede venom. One factor that is likely to be important is the range of different kinds of prey the centipede eats. A species tackling a broad range of prey may be expected to have a greater diversity of toxins than a species specializing in just a particular prey species. By correlating venom composition with the diversity of prey identified in their guts we can begin to answer this question. Lastly, by looking at what kinds of changes have occurred in the toxin sequences, and in which parts of them, we can infer the types and intensities of selection pressures that were most important in shaping toxin diversity.

Publications

10 25 50
 
Description This grant allowed us to generate the first overall insights into the composition and evolution of centipede venoms. Compared to other venomous animals, such as snakes and spiders, very little research has been done on centipede venoms. This is surprising because this diverse group of venomous animals holds great potential to inform our general understanding of venoms. There are 5 main living groups of centipedes, but our understanding of centipede venom is based almost entirely on the study of only one of these 5 groups.

The grant has allowed us to study the venoms from representatives of all 5 groups, and this has provided the most comprehensive knowledge of the overall composition of centipede venoms and there evolution to date. One key finding is that these centipede groups have their own distinctive venoms, and that none can be regarded as representative of the others. Another finding is that centipede venom composition is highly dynamics over macroevolutionary times, involving both increases and decreases in venom complexity. These results are currently being finalised for a peer-reviewed publication.
Exploitation Route This research provided the first comprehensive overview of venom composition across the main groups of centipedes. Our findings may be taken forward academically by researchers interested in further studying this topic. The breadth of our comparative approach has raised new questions, and provides a guide to researchers on what taxa to study next to tackle them. Additionally, our findings about venom composition are a valuable resource for researchers interested in finding novel bioactive compounds to develop into seed compounds for the development of new pharmaceuticals.
Sectors Pharmaceuticals and Medical Biotechnology,Other

 
Description A conference grant from Company of Biologists
Amount £3,000 (GBP)
Organisation Company of Biologists 
Sector Charity/Non Profit
Country United Kingdom
Start 02/2013 
End 02/2013
 
Description DFG postdoctoral grant to study crustacean venoms
Amount € 61,000 (EUR)
Funding ID GZ: RE 3454 
Organisation German Research Foundation 
Sector Public
Country Germany
Start 10/2012 
End 09/2014
 
Description Collaboration on the venom of centipedes and remipedes. 
Organisation University of Queensland
Country Australia 
Sector Academic/University 
PI Contribution Providing research material and analytical skills.
Collaborator Contribution Supplying new research data and analytical skills.
Impact Several publications are in the planning stage.
Start Year 2014
 
Description Investigation of polychaete venoms and remipede venoms 
Organisation University of Leipzig
Country Germany 
Sector Academic/University 
PI Contribution We collected specimens for research and contributed to data analyses.
Collaborator Contribution They collected specimens for research and contributed to data analyses.
Impact Two publications, as listed in the relevant section of Researchfish.
Start Year 2012
 
Description Delivery of temporary exhibition 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact I have developed and delivered, as scientific lead, a major temporary exhibition on venom that runs at the Natural History Museum from November 2017 till mid May 2018. The exhibition has attracted lots of positive media attention and reviews, and has so far attracted more than 28,000 visitors. The exhibition highlights in various places that the museum is actively engaged in researching venoms and venomous organisms, and I have personally given tours to many visitors as well as internal colleagues, and been interviewed in print, radio and tv media.
Year(s) Of Engagement Activity 2017,2018
 
Description Departmental talk at Oxford Brooks University 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact Talk sparked questions and discussion.

No notable impacts.
Year(s) Of Engagement Activity 2014
 
Description Engagement with general audience during open science night at Natural History Museum 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact The open science event myself and my pre-doctoral research assistant participated in is called Science Uncovered and took place on 30 September 2016. It is the NHM's contribution to the EU funded European Researchers' Night. The event was attended by several thousand people, and we engaged a large number of visitors for 3 hours with specimens and video footage related to venomous animals, highlighting our research. People were amazed that venomous animals are not just spiders, scorpions and snakes, and that the world of venom does a lot for society, including seeding the development of new pharmaceuticals.
Year(s) Of Engagement Activity 2016
 
Description Interactive public display of venomous animals during NHM event 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Presented a talk on my centipede and related venom research, followed by a dialogue with general audience members in which I showed them specimens from the NHM collections.

The audience displayed enthusiasm about the new knowledge they gained during my talk.
Year(s) Of Engagement Activity 2014
 
Description Invited talk at the Bangor University Student Entomological Society 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Undergraduate students
Results and Impact I presented an invited talk highlighting my centipede and related venom research for an audience composed mostly of undergraduate university students who are members of the Bangor University Student Entomological Society

The audience members were very eager to discuss after my talk, and i have been re-invited to present a talk in 2015.
Year(s) Of Engagement Activity 2014
 
Description NESCent discussion meeting on animal venoms 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other academic audiences (collaborators, peers etc.)
Results and Impact The discussion meeting resulted in the drafting of several manuscripts that summarise current thinking in areas of venomics research, and explore roadmaps for future research in the community.

Broad internal exchange of ideas between participants with very different background, and the drafting of manuscripts together with participants.
Year(s) Of Engagement Activity 2014
 
Description Presentation for general audience at a pub in Crystal Palace, London 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact I presented a talk on venomous animals and my research on them in a pub in Crystal Palace.
Year(s) Of Engagement Activity 2015
 
Description Presentation for general audience at the Natural History Museum 
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 presented a talk to an audience of about 50 members of the public on venomous creatures, supported by Powerpoint and specimens from the Museum's collections. This included highlighting my research on centipedes and venomous polychaetes.
Year(s) Of Engagement Activity 2015
 
Description Presentation for general audience at the Natural History Museum 
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 presented a talk to an audience of about 50 members of the public on venomous creatures, supported by Powerpoint and specimens from the Museum's collections. This included highlighting my research on centipedes and venomous polychaetes.
Year(s) Of Engagement Activity 2015
 
Description Presentation to A level students at the Natural History Museum 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact I presented a talk with Powerpoint and specimens from the Museum's collections to a group of A level students, highlighting my work as a researcher.
Year(s) Of Engagement Activity 2016
 
Description Public talk about venomous organisms and my venom research 
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 presented a specimen assisted talk to visitors of the Museum about venomous animals and my venom research.

I enthused the audience.
Year(s) Of Engagement Activity 2014
 
Description Science Uncovered 2017 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact I participated and discussed my ongoing research at the yearly EU funded researchers night, which we call Science Uncovered at the NHM, on the last Friday of September. The activity consisted of showing specimens and discussing the world of venom with the general public who were surprised that the museum is engaged in such exciting scientific research.
Year(s) Of Engagement Activity 2017
 
Description Talk about venom research for general audience at the Natural History Museum 
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 presented an interactive talk on my centipede and related venom research, as well as general aspects of the biology of animal venoms for a general audience, showing real specimens.

No notable impact other than enthusiasm displayed by the audience members.
Year(s) Of Engagement Activity 2013