Population genomic tests for mechanisms of ecological speciation in bdelloid rotifers

Lead Research Organisation: Imperial College London
Department Name: Life Sciences

Abstract

Sex is nearly ubiquitous among animals. Most animals have a stage in their life-cycle when genes from different individuals are shuffled to produce genetically mixed offspring. By doing so, natural selection acts more efficiently both to remove harmful mutations from populations and to allow beneficial combinations of genes to spread. Sex also has profound implications for speciation, namely how an ancestral species diverges into separate descendent species. Adaptation to different habitats and isolation in separate geographical areas can promote speciation, but a key step for sexual organisms is to acquire genetic or behavioural traits that prevent gene exchange. As a result, most speciation research has focused on reproductive isolating mechanisms that restrict gene exchange between diverging populations.

Some organisms defy the general ubiquity of sexual reproduction. Bdelloid rotifers are microscopic animals that live in freshwater, such as ponds and the water film on mosses. No males or cellular signs of sex have ever been found, and recent genomic evidence indicates that their chromosome structure is incompatible with the normal pairing of chromosomes associated with sex. Despite the presumed costs of such a lifestyle, bdelloids comprise hundreds of morphologically distinct species. Our previous work confirmed that bdelloids have diversified into independently evolving groups akin to species and found evidence for morphological adaptation to different habitats. But what mechanisms led to divergence? Have bdelloids really evolved as asexuals or do they have hidden mechanisms for gene exchange?

One recent discovery found another weird feature of bdelloids that might contribute to adaptation to different environments. Bdelloids harbour thousands of genes that appear to derive from bacteria, protists, plants and fungi and have been taken up into the bdelloid genome where they provide new functions. Some of those functions are previously unknown in the metabolic repertoire of animals. It is believed that uptake occurs (rarely) when bdelloids repair their DNA following damage caused by desiccation - another weird feature of bdelloids is their ability to survive desiccation, a stress that kills most other animals. The uptake of foreign DNA is well known in bacteria, where it contributes to specialisation to different niches (e.g. to cause disease in a new host), but the levels in bdelloids are unprecedented among animals. Might the uptake of foreign genes provide a way for bdelloids to acquire new functions and adapt to different environments, as in bacteria? Or perhaps there are other hidden mechanisms of gene exchange between bdelloids?

We will use genome sequencing to test the importance of gene exchange and the uptake of foreign DNA in 4 closely related bdelloid species living in different habitats: 2 species in habitats that desiccate regularly and 2 that are fully aquatic and cannot recover from desiccation. Our prior work found that most foreign genes are shared, but a significant remainder appear to be unique to each species. We will sequence whole genomes to verify or refute the status of these genes. We will also sample genomic variation within each species to test whether shuffling of genes has occurred, and if so whether that conforms to hidden sexual exchange (unlikely) or other mechanisms. We will test whether gene exchange has shaped the pattern of natural selection across genes. The results will reveal the contribution of strictly asexual evolution versus gene exchange in bdelloid adaptation and speciation. Findings for these intriguing animals will contribute new knowledge of mechanisms that promote adaptation and speciation, in comparison to organisms with more conventional lifestyles.

Planned Impact

Who will benefit from this research?

This proposal focuses on discovery of fundamental evolutionary processes and their action in an unusual set of animals. The main beneficiaries outside academic circles will be the general public. Additional benefits will be training of skilled workers in bioinformatics and genomics for future careers that might lie in government or industry as well as in academia. There are possible future benefits of our genome databases to aid bioprospecting for genes involved in DNA repair, although these are unlikely to be direct benefits here.

How will they benefit?

The public will benefit from learning about evolutionary mechanisms, genomics and speciation made palatable by the curious lifestyles of bdelloids (microscopic, asexual, surviving desiccation), enhancing culture and knowledge. Bdelloids have enjoyed considerable media exposure over the last 15 years, evidence of public interest in media releases on this topic. They will benefit from the start and especially years 2 onwards of the project.

Potential future employers will benefit from staff trained to a high level in areas representing skills gaps in the UK (e.g. bioinformatics). After the lifetime of the grant (or after year 1 for the associated technician).

Comparison of gene sets in desiccating and non-desiccating bdelloids might reveal potential targets for storing biological material or gene therapy against DNA damage. (very unlikely within the lifetime of the grant).
 
Description We isolated genomic DNA from 5 species of rotifers and we prepared those for submission for sequencing.

We submitted a manuscript entitled "Comparative genomics of desiccating and non-desiccating species of bdelloid rotifers" to PLoS Biology, which is now published. This paper showed that the main unique feature of bdelloid genomes is their high levels of horizontal gene uptake. Other features reported in the 1st bdelloid rotifer genome were not supported by the new data. The work provided a platform for our subsequent investigations

We have obtained resequencing data for 2 species that is being used for population genetic tests in recombination, selection and horizontal transfer. We have now assembled a dataset of 27 new genomes, including 4 species with 5 resequenced individuals, and a draft paper with the first analyses is now accepted in eLife. One more paper focusing on these samples is now in preparation.
Exploitation Route The genomes will also be available to other researchers interested in comparative genomics upon publications. We received funding for a new grant on bdelloid coevolution with parasites and the genomes provide the strong basis for genetic analyses in that project.
Sectors Environment

URL https://elifesciences.org/articles/63194https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.2004830
 
Description We presented our science at the Science Museum Lates in February 2016 on Sexuality and at BUGS day 2016, 2017, 2018, and at school outreach days at Magdalen College Oxford in 2020.
Sector Environment
Impact Types Cultural

 
Description The genomic basis of adaptation to virulent pathogens in asexual bdelloid rotifers
Amount £438,251 (GBP)
Funding ID NE/S010866/2 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2019 
End 02/2022
 
Title Genome sequence data 
Description Assemblies of genome sequence data for 3 bdelloid rotifer species: A.ricciae, R.magnacalcarata and R. macrura. 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
Impact Publication in revision. 
URL https://www.ebi.ac.uk/ena/data/view/PRJEB23547
 
Title Genome sequence data from Nowell et al. 2021 Elife 
Description Genome read data, assemblies and gene predictions for 26 new rotifer genome sequences reported in Nowell et al. 2021 Elife 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
Impact Greatly expanded from 3 earlier genomes available for rotifers, increasing knowledge of this part of animal phylogenetic tree considerably. 
URL https://elifesciences.org/articles/63194
 
Description Prof Alan Tunnacliffe and Dr Chiara Boschetti 
Organisation University of Cambridge
Country United Kingdom 
Sector Academic/University 
PI Contribution We collaborated to assemble genome sequence data for Adineta ricciae generated by Prof Tunnacliffe and Dr Boschetti
Collaborator Contribution They generated the sequence data for Adineta ricciae
Impact Manuscripts already reported on research fish from earlier grants; manuscript in revision. Partnership brings together biochemistry and molecular biology with evolutionary biology and bioinformatics.
Start Year 2007
 
Title Comparative genomic pipelines 
Description Bioinformatic pipelines for comparative genomics including for identifying horizontal gene transfer and for inferring collinearity for multiple genomes. Made available by post-doc Dr Reuben Nowell on GitHub 
Type Of Technology Software 
Year Produced 2019 
Open Source License? Yes  
Impact 490 downloads since deposition 
URL https://github.com/reubwn
 
Title Transposable element evolution pipeline 
Description Pipeline of software to find transposable elements within genomes, and compare various aspects of their evolution among multiple species. 
Type Of Technology Software 
Year Produced 2021 
Open Source License? Yes  
Impact Pipeline for other researchers 
URL https://github.com/reubwn/te-evolution
 
Description BUGS day 2018 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Public science event at Imperial's Silwood Park campus, attended by around 500 members of public, largely families with children. My exhibit had microscopes showing bdelloid rotifers and explaining aspects of their lifestyle and our research findings.
Year(s) Of Engagement Activity 2018
URL http://www.imperial.ac.uk/ecosystems-and-environment/news-and-events/gcee-outreach/bugsday/
 
Description Outreach event to schools 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Schools
Results and Impact Outreach events to students from year 10 and 11 from 5 schools in Westminster and 1 school in Ashfield (Notts), presenting the rotifer example of asexual evolution and engaged in a discussion session with pupils.
Year(s) Of Engagement Activity 2020
 
Description Public display at Bugs Day 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact This is an open day focused on families and schools for finding out about science we do on campus, with a nature theme to attract local wildlife organisation etc as well.
Year(s) Of Engagement Activity 2016
URL https://www.youtube.com/watch?v=nlTLHz-pFPM
 
Description Public open event - BUGS day 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Our annual public science day, this year was attended by 500 people, many of them families with children. We had a stall with microscopes demonstrating bdelloid rotifers and explaining about their asexuality and our genome sequencing project. Two Masters students who completed projects in the lab affiliated with this award helped me to man the stall.
Year(s) Of Engagement Activity 2017
URL http://www.imperial.ac.uk/ecosystems-and-environment/news-and-events/gcee-outreach/bugsday/
 
Description Science Lates event at Science Museum 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact We presented a stall at the Science Museum Lates event on Sexuality. We had bdelloid rotifers for people to view under the microscope, and slides presenting key information about bdelloid asexuality and its significance for their evolution. The stall was visited by many 100s of people over the evening who found out about evolutionary basis for sex versus asexuality and asked questions.
Year(s) Of Engagement Activity 2016
URL http://www3.imperial.ac.uk/newsandeventspggrp/imperialcollege/eventssummary/event_22-1-2016-17-47-33