Beyond the Red Queen: are elevated parasite evolutionary rates driven by host shifts?

Lead Research Organisation: University of Liverpool
Department Name: Sch of Biological Sciences

Abstract

Evolution is change over time. Most people know of evolution in terms of responses to man-made influences - bacteria evolve resistance to antibiotics; industrial pollution led to the evolution of dark forms of the peppered moth. However, in natural systems, evolution is most rapid in genes that contribute to parasite infectivity and to the ability of the organisms they infect to stop parasites from propagating. Forty years ago, Leigh Van Valen produced a theory as to why genes involved in parasite infectivity and host resistance should evolve more quickly than others. This theory noticed that evolution would be rapid where there was 'mutual antagonism'. Hosts evolve to resist infection by parasites, so parasites must adapt to circumvent this resistance (or die). Reciprocally, as the parasites adapt to better infect their hosts, so the hosts must adapt (or die). This creates a continual cycle termed antagonistic coevolution, where parasite virulence and host defence genes continually adapt, and counter adapt, in an arms race. This continuous 'catch up' between hosts and parasites parallels a scene from Lewis Carrol's famous book, Through the Looking Glass, in which Alice (a.k.a. Alice in Wonderland) runs rapidly with the evil Red Queen, yet gets nowhere. Red Queen interactions are widely accepted as 'the' reason why genes involved in host defence and parasite virulence evolve quickly. However, it is possible that it is only a partial explanaiton. This proposal seeks to test an alternative explanation for fast evolution of parasite genes rarely examined to date: parasite virulence genes evolve rapidly because parasites occasionally switch host species. Host switching occurs quite commonly in parasites. We have all heard about it- HIV moved from primates into humans about 70 years ago, and Swine Flu and Avian flu have raised our awareness of new influenza shifting from pigs and birds into humans. It is likely that host switching by a parasite represents a very strong selective force. Following a host switch, the entire environment of the parasite is different, and a parasite in its new host is likely to perform poorly. Thus, there is great scope for adaptation of the parasite to its new host, and it must rapidly evolve to better exploit the host. It is clear that parasites do 'switch' hosts quite commonly, and very likely this is accompanied by a bout of strong natural selection that may explain why parasite 'virulence' genes evolve rapidly. In this project, we will test the theory that host shifts drive fast parasite evolution. In the laboratory, we will produce host shift events for a bacterium, moving the bacterium from its native host into a new 'foreign' one. We will leave this bacterium in its new host species for a year, and then recover it. We will investigate whether the host shift has resulted in the bacterium evolving more quickly in terms of gene sequence, and whether it has evolved in terms of its ability to prosper in its new host. We will also examine the diversity of the bacterium across host species which it has colonised through host switching in nature. By comparing the differences seen between bacterial strains in the wild to those following laboratory host shifts, we can ask if natural diversity is likely driven by the host shift events it has encountered in the past

Publications

10 25 50
 
Description We have found Arsenophonus in European Nasonia for the first time, We have demonstrated a novel population biology for Arsenophonus based on host co-parasitism rates that we have published.
We have demonstrated that Arsenophonus ability to invade a host is a property of:
a) host biology/ecology, in terms of superparasitism rate
b) host biology, in terms of transmission efficiency and cost of infection in novel hosts.
In addition, we have shown that Arsenophonus does not rapidly evolve when placed in a new host species. This is unusual, in that microbes usually evolve rapidly when they switch host species.
We have further determined that Arsenophonus nasoniae is the most phage rich microbial genome sequenced to date.
We have further demonstrated that the clade Arsenophonus:
a) Contains species closely related to that in Nasonia, but which do not kill males.
b) these non-male-killers have very similar genomes to the male-killers, indicating male-killing is a few significant changes.
c) Contains a group associated with honey bees, and poor honey bee health.
Exploitation Route Establish which symbiont genes are important in symbiont-host interaction, important in establishing use of symbionts in natural populations (follow on funding x3)

Improvement in honey bee health/diagnostics (follow on funding x 2)
Sectors Agriculture, Food and Drink,Environment

 
Description To establish a collaboration with FERA to investigate symbiont impacts in bee health, an economic and biodiversity issue.
First Year Of Impact 2014
Sector Agriculture, Food and Drink,Education,Environment
Impact Types Societal,Economic

 
Description BES
Geographic Reach National 
Policy Influence Type Membership of a guidance committee
Impact Member of BES Education committee, advising on changes in GCSE and A level curricula to Department of Education through SCORE
URL http://www.publications.parliament.uk/pa/cm201213/cmselect/cmeduc/141/141we22.htm
 
Description BBSRC iCASE
Amount £94,000 (GBP)
Funding ID BB/L016133/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 10/2014 
End 09/2018
 
Description EMBO Long Term Fellowship (COFUND)
Amount £31,000 (GBP)
Funding ID EMBO/ALTF/48-2015 
Organisation European Molecular Biology Organisation 
Sector Charity/Non Profit
Country Germany
Start 10/2015 
End 10/2016
 
Description EU Marie Curie Global Fellowship
Amount € 241,169 (EUR)
Funding ID BEESYMOVERSPACE 
Organisation European Commission 
Sector Public
Country European Union (EU)
Start 08/2016 
End 03/2019
 
Description Establishing the genetic basis of symbiosis in an insect host
Amount £605,110 (GBP)
Funding ID BB/S017534/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 06/2019 
End 06/2022
 
Description H2020 Marie Curie Fellowship
Amount € 180,000 (EUR)
Funding ID SymMech 
Organisation European Commission 
Sector Public
Country European Union (EU)
Start 01/2017 
End 12/2019
 
Description Marie Curie Europe Fellowship
Amount € 186,000 (EUR)
Funding ID SYMCOMPAT 
Organisation European Commission 
Sector Public
Country European Union (EU)
Start 10/2016 
End 09/2018
 
Description Newton Grants for ODA
Amount £100,000 (GBP)
Funding ID 275898413 
Organisation British Council 
Sector Charity/Non Profit
Country United Kingdom
Start 04/2017 
End 03/2018
 
Title A. nasoniae genome data 
Description The complete genome sequence for A. nasoniae, and analysis therein. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
Impact Complete genome resource for this model insect symbiont 
URL https://www.ncbi.nlm.nih.gov/bioproject/529362
 
Description Beesymbionts 
Organisation Fera Science Limited
Country United Kingdom 
Sector Public 
PI Contribution Establishment of Industrial CASE project to investigate symbiont influences on bee health
Collaborator Contribution Expertise; data; bee facilities
Impact BBSRC iCASE studenthsip
Start Year 2014
 
Description USDA 
Organisation U.S. Department of Agriculture USDA
Department Beltsville Agricultural Research Center
Country United States 
Sector Academic/University 
PI Contribution UK-USA collaboration to perform geographical comparison of Arsenophonus-honey bee interactions.
Collaborator Contribution Host for Global Marie Curie fellow; provision of USA data for collaboration
Impact Marie Curie Global fellowship, hosted by University of Liverpool, for PDRA Crystal Frost to spend 22 months at USDA ARS with Dr Jay Evans, and then return to UK for 12 months.
Start Year 2016
 
Description Association of Science Educators, Talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact Gave talk on 'Microbes in Animal life' to the 'Fronteirs of Science' Symposium at the Association of Science Educators.
Generated questions during the talk, email enquiries for materials after the talk, and positive feedback on feedback forms.
Year(s) Of Engagement Activity 2016
URL http://www.ase.org.uk/ase-regions/north-east-midlands/events/2016/01/06/1537/
 
Description BES education committee 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact BES education committee extends the British ecological society remit into the practice of education. The committee on which I served:
a) establish Doctoral Training programme training schemes used by the NERC DTP ACCE
b) advised government on education reform policy at GCSE and A level, including curriculum design and assessment
c) established undergraduate summer schools for ecological education.
Year(s) Of Engagement Activity 2012,2013,2014,2015
 
Description Lecture to Secondary school science teachers 
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 Lecture to Science educators conference in 'Science in the Real World' programme, on microbial importance in animal biology, ecology and evolution. Interest afterwards via email; potentially to be made into podcast for the British Ecological Society Engagement series.
Year(s) Of Engagement Activity 2016
 
Description LeedsSchoolvisit 
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 2 day introduction to minibeasts sessions for KS1 and KS2 at school in deprived neighbourhood.

Positive feedback from pupils and teachers
Year(s) Of Engagement Activity 2014
 
Description School visit (Birkenhead) 
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 40 Reception pupils and 15 Science club students on MiniBeast adventure activity

Features in school newsletter
Year(s) Of Engagement Activity 2014
URL http://issuu.com/birkenheadschool/docs/infocus_obsbulletin2014?e=8039437/8912683
 
Description School visit (Pinfold) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? Yes
Geographic Reach Local
Primary Audience Schools
Results and Impact KS1 and KS2 bug hunt day. Lots of positive feedback.

Continued partnership.
Year(s) Of Engagement Activity 2013
URL http://www.bonkers-bugs.co.uk/p/rolls-royce-finalist-prize.html