Genetics and evolutionary dynamics of male-killer suppression in the lacewing, Mallada desjardinsi

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

Abstract

Evolution has historically been thought of as a slow process, happening over geological time periods. However, we now know that contemporary evolution can in fact be very fast, with new genetic types (mutations) spreading rapidly through natural populations. One case where evolution is particularly quick is the response of insect populations to male-killing bacteria. Many insect species carry these microbes - which do exactly what their name suggests -kill only male carriers (and leave females unharmed). They pass from a female (mother) insect into sons and daughters - and kill the sons.

Natural selection, of course, promotes mutations in insects that rescues these males. These rescue mutations are known in four different cases now. In 2007, we were fortunate enough to observe one of these rescue genes spread in nature through a population of butterflies. Before the rescue mutation spread, male-killing bacteria were so common and effective there were 100 females to every male butterfly. After the spread of the rescue element, males and females equally common. The rescue mutation spread through the population in under a year - 10 butterfly generations. Further research has also told us how rescue works - the mutation makes male butterflies in a different way that stops them being killed.

Recent work by a Japanese group observed the same type of evolutionary event in a different bacteria/insect interaction in a different part of the world. Here, the insect was a lacewing, and the male rescue mutation took 4-5 years to establish - very fast even if not quite as quick. We call these independent but similar events cases of convergent evolution - and they allow us a wonderful opportunity into understanding whether natural selection takes the same route to 'solve' the same problem - and whether evolution in response to these parasites hits a single aspect of host biology - or many.

This study will examine this study system in order to determine if the outwardly similar event (evolution to rescue males) has the same target or whether these evolutionary events actually involve many different aspects of male/female development. We will use state of the art genomic technology to determine whether the gene changes that rescue male lacewings are of the same kind that rescue male butterflies.

Further, we can ask if the dynamics of these super fast evolutionary events is the same in different cases - or whether it depends on the properties of the particular symbiont. We predict it will be different in this case, as the symbionts affect on the host differ in some important ways.

Finally, we ask if the rescue mutation affects the fertility and fecundity of male and female adults. If it does, then this implies that how male and females are is not simply a product of sexual selection - of competition for mates or selection to produce offspring - but also selection to avoid sex specific parasitism.

The team brings together complementary skills. The Japanese group brings expertise of the study system, and vital historical samples and data that allow us to infer evolution directly. The UK group brings expertise in the genetic analysis of evolutionary change. Together, they can solve a long standing puzzle.

Planned Impact

Biological control companies represent the principle non-academic group that will benefit from this research. Lacewings are voracious predators that are widely mass cultured and sold to help control aphid and lepidoptera pests. The genomic resources developed in this project will represent the first for a lacewing. In parallel with other systems, developing genomic understanding allows more targeted development and breeding of strains that will be more efficacious in biocontrol. For instance, the male-killing trait under study may be harnessed to improve mass culture, where the size of the female population is key for productivity. The genetic markers and genomic knowledge may additionally be used to develop more efficient strains in application in glass house and field settings.

Together, the resources would allow biocontrol to reduce the per unit cost of production of this agent, and the efficiency with which it supplies control.

UK competitiveness will also benefit from this research in terms of providing new collaborations with Japanese investigators, and training of early career scientists in next generation sequencing and bioinformatic skills that are becoming widely used in health and food science research.
 
Description We are investigating a case of rapid evolution in response to a parasite - a bacterium that kills male insects and a mutation in the lacewing that rescues them. We have observed that despite the spread of the male-killer suppressor mutation, the bacterium has not declined in frequency.

We have sequenced the genome of Mallada desjardinisi and its associated symbionts to high quality. This has been annotated with RNAseq data to produce a polished genome.

We have recovered the genomic region associated with suppression of male-killing. Interestingly, this is different from the locus identified in other species.

We have completed the genome sequence for the male-killing Spiroplasma, which is the largest in its clade. The genome expansion is due to a proliferation of mobile repetitive elements. Interestingly, we observed the same pattern for a Rickettsia symbiont in the same clade.

We have discovered a non-suppressible Spiroplasma strain - one that retain male-killing even in the presence of the suppressor. This is the first record of variation in symbiont capacity to be suppressed, which is important in terms of understanding dynamics. A prediction is that this strain will now spread in competition with the strain that can be suppressed.

We are currently investigating the population genomic variation found in the symbiont population
Exploitation Route To discover what other mechanisms maintain the parasite in the population.
To understand how the resistance mutation works, and what it reveals about the phenotype of male-killing.
Sectors Agriculture

Food and Drink

Environment

 
Description Insect cell culture systems to explore the symbiont-sex determination system interface.
Amount £200,000 (GBP)
Funding ID BB/Y513209/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 02/2024 
End 09/2025
 
Description NARO Japan 
Organisation National Institute of Agrobiological Science, Japan
Country Japan 
Sector Academic/University 
PI Contribution This project is a joint venture between NARO Japan and the UK. The UK team provide genomics expertise.
Collaborator Contribution NARO partners work with insect collection and breeding work, and expertise on the model system
Impact The grant itself is an outcome
Start Year 2019
 
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 Interview on local news 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Media (as a channel to the public)
Results and Impact 10 minute interview on Radio Merseyside on insect related issues, viz ladybird sightings and mosquito biting activity in the local area.
Year(s) Of Engagement Activity 2023