How do sex ratio distorting symbionts affect the evolution of their host?

Lead Research Organisation: University of Liverpool
Department Name: Institute of Integrative Biology

Abstract

The biology of animals is in part a function of the microbes they interact with. During digestion, for instance, food is broken down both by enzymes secreted by our digestive system and those secreted by the microbes that live within the gut. In many insects, microbe-host interactions are even more developed. Bacterial symbionts live inside the cells of the insect body, and these are passed from a female to her offspring via her eggs: heritable symbiosis.

We know a lot about how these symbionts affect the individual they infect. One particularly interesting impact is male-killing, where the bacterium passes from a female to her eggs, and kills those which develop as males. We know male-killing bacteria are common: they are present in many species, and, where they are present, can be present in the majority of individuals - this produces insect populations where males are rare. However, we know little about how these bacteria affect insect ecology or evolution. A variety of researchers believe these symbionts may drive changes in the way male and female insects are formed during development, sex determination. The hypothesis is simple - where symbionts target males only, natural selection counteracts this by favouring new ways of making a male that escape male-killing.

This study will examine this theory for a recent case of evolution of the blue moon butterfly to avoid the action of male-killing bacterium called Wolbachia. We have documented the spread of a mutation that rescues male blue moon butterflies from Wolbachia-induced death. This project will establish what this mutation is, whether it involves changes in a gene called 'doublesex', which defines male and female characteristics in insects.

A second aspect of male-killers is that they may drive very strong natural selection to rescue males. The intensity of selection is such that the changes that occur to rescue males may be otherwise deleterious. A second aim of the project is to establish if this is true, and whether the mutation (beyond rescuing males) degrades male and female function.

In completing this project, we will present the first direct test of the theory that the processes that make males/females different can be driven by microbes. This is an enigmatic link that would make clear the interdependence of insect and microbe evolution.

Planned Impact

This system represents a spectacular case study of evolution in action, which involves both an attractive insect species and an intriguing parasite. This produces impact opportunities in the communication of science: because this is a study system in which we have observed natural selection, the research permits us to establish natural selection as an ongoing observable process, rather than a theory from which we can infer support, or as a long term process we cannot observe - a common misconception that raises skepticism over the process occurring at all. The importance of the study system in this communication is reflected in past work featuring as a front page story on Yahoo. The work also raises the topical issue of how 'male' and 'female' are defined, which is another aspect of biology very accessible to the public.

Who will benefit from this research?
a) Public sector/Third sector: Museum, Zoo and butterfly house educational facilities
b) Wider public
c) UK economic competitiveness

How will they benefit from this research?
a) Production of displays and lectures relevant to museum exhibitions on evolution, and to butterfly houses/zoos in which Hypolimnas butterflies are flying.
b) General public/society through increased science literacy: the key message for translation within this proposal is that evolution is an ongoing process rather than a purely historical phenomenon. This knowledge is required for assessment of impact of anthropogenic change in the medium term, which is required to evaluate policy and priorities with respect to this form of change.
c) UK economic competitiveness through training of researchers in leading genomic technologies used in biotech and health R&D.
 
Description We are examining the genetic basis of resistance to a male-killing parasite.
We have identified a candidate gene, doublesex, that appears likely to be the target of selection.
This would drive evolution of the genetic systems that make male and female distinct.
Thus, male and femaleness in insects may in part be a response to parasites that target one sex alone.
We have additionally determined that a single locus is required for male rescue - there appears to be a single mutation event required. This was surprising, as it took a long time for suppression to evolve.
Finally, we have completed a draft genome sequence for the butterfly, and the microbe, to identify changes that occurred alongside suppression spread.
Exploitation Route Exploration in other systems to examine the generality of the finding would be appropriate.
Sectors Environment

 
Description Genetics and evolutionary dynamics of male-killer suppression in the lacewing, Mallada desjardinsi
Amount £445,408 (GBP)
Funding ID NE/S012346/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 02/2019 
End 02/2022
 
Description Thailand Government
Amount £105,000 (GBP)
Funding ID 5302.3/1157 
Organisation Institute for the Promotion of Teaching Science and Technology 
Sector Public
Country Thailand
Start 10/2017 
End 09/2020
 
Title Hypolimnas physical genetic marker set 
Description A set of markers that can be used to map traits in this buttefly 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
Impact Allows other users to map traits in this species simply. 
 
Description Darryl Kemp 
Organisation Macquarie University
Country Australia 
Sector Academic/University 
PI Contribution To come
Collaborator Contribution Field collection of butterflies; measurement of wing spectral quality.
Impact To come
Start Year 2017
 
Description Art activity for children centred on project 
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 120 children aged 3-15 attended art workshops based on our butterfly, and learnt about insect life cycles. We taught the parents about microbes and how they impact the health of insects and humans.
Year(s) Of Engagement Activity 2019
URL https://blogandlog.wordpress.com/2019/07/08/butterfly-crafternoon-at-the-williamson/
 
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 BBC Gardener's question time 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact As part of BBC Gardener's Question Time annual garden party at Ness Botanic gardens, helped to man a stall with colleagues where I spoke with members of public about our research project.
Year(s) Of Engagement Activity 2017
 
Description Film Introduction 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Gave an introductory talk for a screening of Alfonso Cuarón's 2006 film 'Children of Men' at a local film club. During this talk I discussed the science behind the themes of this film.
Year(s) Of Engagement Activity 2017
 
Description School visit (Salford) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Presentation to year 12 student on careers in Research Science
Year(s) Of Engagement Activity 2017
 
Description Stratford-Upon-Avon butterfly farm 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Having formed a collaboration with Stratford-Upon-Avon butterfly farm, as part of our research project we performed outreach activities to engage with visitors to the farm, whilst doing butterfly breeding. We spoke with many members of the public of all ages about butterflies and the work that we are doing.
Year(s) Of Engagement Activity 2017