The evolution of female mating systems: tracing the origins and tracking the consequences
Lead Research Organisation:
University of Stirling
Department Name: Biological and Environmental Sciences
Abstract
A key focus in evolutionary biology has been to understand how mating patterns evolve in different species and populations. Research into mating behaviour has historically focussed on why extravagant male traits evolve, but in recent years more subtle aspects of female mating behaviour have been uncovered. Traditionally females were assumed to mate only once (monandry) to acquire enough sperm to reproduce. However, it is now clear that monandry is rare and that females typically mate with multiple males (polyandry). Recent work has shown that while polyandry can be costly, it can also allow females to produce more offspring, and that polyandrous populations can be less likely to go extinct. Yet, while we know that female preference can drive evolutionary change in extravagant male traits (like the peacock's tail), we still do not know what drives the evolution of different female mating rates and why monandry is so rare. The work that I propose will advance our understanding of female mating strategies, broadening the field to ask questions about how and why female mating systems change.
I will develop simulation models (collab. Dr Brad Duthie) to infer how many times the first sexually reproducing organisms, which lived billions of years ago, mated. These models will help me to understand how mating patterns in ancient organisms evolved alongside sexual reproduction, in terms of the evolution of separate sexes (males and females) and internal fertilisation (mating).
I will then construct an evolutionary model to look at finer scale and more recent changes in female mating behaviour in a novel group of species, the parasitoid wasps. Parasitoid wasps are important natural enemies that are used to control pest species, so we know a lot about their behaviour, physiology and genetics. In particular, parasitoid females have diverse mating rates across different species ranging from asexuality (no-mating) through to monandry and polyandry.
The diversity in and knowledge of female mating patterns across the parasitoids will allow me to use evolutionary analyses to estimate when and why female mating behaviour changed in the past, and whether these changes drive the evolution of other traits (collab. Dr Sally Street). As an example, parasitoids show great variation in the sex ratio; in some species over 90% of the population are female. I predict that polyandry will be more common in species with strongly female-biased sex ratios, so that females can obtain enough sperm to reproduce.
I will also track changes in female mating behaviour in real-time using experimental evolution in the aphid parasitoid Lysiphlebus fabarum (collab. Prof Christoph Vorburger). I will run experiments at the University of Stirling, setting up greenhouse populations comprised of monandrous, polyandrous and asexual females and then alter the sex ratio, to either limit or increase the availability of males. I will measure female mating rates over generations to test whether factors such as mate-limitation drive changes in the frequency of different female mating strategies.
My results will reveal whether polyandrous, monandrous or asexual parasitoids are likely to be more robust to extinction threats (such as climate change). These findings also have important ramifications for the control of pests and invasive species by parasitoid wasps and could be used to develop long-term sustainable and cost-effective biological control strategies in order to control crop pests and invasive species. The international partnerships that I have developed (Dr Luc Bussiere, Dr Bart Pannebakker) will facilitate the dissemination of my findings to industrial stakeholders so that my insights can be integrated into policy.
Alongside my experimental work, I will also use bibliometric techniques to analyse research papers and investigate how integrating new methods and more diverse gender perspectives has shaped our understanding of female mating behaviour.
I will develop simulation models (collab. Dr Brad Duthie) to infer how many times the first sexually reproducing organisms, which lived billions of years ago, mated. These models will help me to understand how mating patterns in ancient organisms evolved alongside sexual reproduction, in terms of the evolution of separate sexes (males and females) and internal fertilisation (mating).
I will then construct an evolutionary model to look at finer scale and more recent changes in female mating behaviour in a novel group of species, the parasitoid wasps. Parasitoid wasps are important natural enemies that are used to control pest species, so we know a lot about their behaviour, physiology and genetics. In particular, parasitoid females have diverse mating rates across different species ranging from asexuality (no-mating) through to monandry and polyandry.
The diversity in and knowledge of female mating patterns across the parasitoids will allow me to use evolutionary analyses to estimate when and why female mating behaviour changed in the past, and whether these changes drive the evolution of other traits (collab. Dr Sally Street). As an example, parasitoids show great variation in the sex ratio; in some species over 90% of the population are female. I predict that polyandry will be more common in species with strongly female-biased sex ratios, so that females can obtain enough sperm to reproduce.
I will also track changes in female mating behaviour in real-time using experimental evolution in the aphid parasitoid Lysiphlebus fabarum (collab. Prof Christoph Vorburger). I will run experiments at the University of Stirling, setting up greenhouse populations comprised of monandrous, polyandrous and asexual females and then alter the sex ratio, to either limit or increase the availability of males. I will measure female mating rates over generations to test whether factors such as mate-limitation drive changes in the frequency of different female mating strategies.
My results will reveal whether polyandrous, monandrous or asexual parasitoids are likely to be more robust to extinction threats (such as climate change). These findings also have important ramifications for the control of pests and invasive species by parasitoid wasps and could be used to develop long-term sustainable and cost-effective biological control strategies in order to control crop pests and invasive species. The international partnerships that I have developed (Dr Luc Bussiere, Dr Bart Pannebakker) will facilitate the dissemination of my findings to industrial stakeholders so that my insights can be integrated into policy.
Alongside my experimental work, I will also use bibliometric techniques to analyse research papers and investigate how integrating new methods and more diverse gender perspectives has shaped our understanding of female mating behaviour.
Technical Summary
The work that I propose will advance current mating systems research, questioning existing perspectives to go beyond asking what maintains the female mating rate, to discover what drives its evolution.
Understanding how populations are structured with respect to sexual interactions (the mating system) has been a key focus in evolutionary biology. Recent scientific insights have revealed that polyandry (multiple-mating by females), and not monandry (single-mating) as traditionally assumed, is the dominant female mating system across specie.
Research on insects has contributed greatly to this paradigm-shift, revealing important factors that maintain female mating rates. Progress in understanding broader patterns has been relatively slow however, as few studies have sought to elucidate evolutionary changes in female mating rates over time.
In this project, I consider evolutionary changes in female mating systems over different time scales using computer simulation and phylogenetic modelling and experimental evolution. I will use individual-based simulations to model the co-evolution of key sexual traits and mating systems in early sexually reproducing organisms. I will track subsequent transitions and reversals from a macroevolutionary perspective in the parasitoid wasps. The great diversity in female mating rates and life-history strategies make parasitoids ideal for testing novel predictions about the evolution of mating systems using phylogenetic modelling. I will complement this phylogenetic work with experimental evolution to track changes in the female mating rate in real-time, under mate-limitation and sexual conflict, in the aphid parasitoid Lysiphlebus fabarum. Alongside my empirical and theoretical work, I will consider the epistemology of polyandry research, asking how diverse methodologies and gender perspectives have initiated challenges to untested dogma and shaped the field.
Understanding how populations are structured with respect to sexual interactions (the mating system) has been a key focus in evolutionary biology. Recent scientific insights have revealed that polyandry (multiple-mating by females), and not monandry (single-mating) as traditionally assumed, is the dominant female mating system across specie.
Research on insects has contributed greatly to this paradigm-shift, revealing important factors that maintain female mating rates. Progress in understanding broader patterns has been relatively slow however, as few studies have sought to elucidate evolutionary changes in female mating rates over time.
In this project, I consider evolutionary changes in female mating systems over different time scales using computer simulation and phylogenetic modelling and experimental evolution. I will use individual-based simulations to model the co-evolution of key sexual traits and mating systems in early sexually reproducing organisms. I will track subsequent transitions and reversals from a macroevolutionary perspective in the parasitoid wasps. The great diversity in female mating rates and life-history strategies make parasitoids ideal for testing novel predictions about the evolution of mating systems using phylogenetic modelling. I will complement this phylogenetic work with experimental evolution to track changes in the female mating rate in real-time, under mate-limitation and sexual conflict, in the aphid parasitoid Lysiphlebus fabarum. Alongside my empirical and theoretical work, I will consider the epistemology of polyandry research, asking how diverse methodologies and gender perspectives have initiated challenges to untested dogma and shaped the field.
People |
ORCID iD |
Rebecca Boulton (Principal Investigator / Fellow) |
Publications
Description | I found that asexual females of the parasitoid wasp Lysiphlebus fabarum are still able to reproduce sexually (facultatively sexual reproduction). When an asexual female mates she can produce some offspring sexually and some asexually (within the same brood of offspring). Some of her offspring are triploid and possibly sterile, others are fertile. |
Exploitation Route | Studies on the use of Lysiphlebus fabarum as a biocontrol agent of aphids - testing whether integrating new genetic material into commercially reared lines through facultative sex can improve control when aphids evolve resistance to biocontrol. |
Sectors | Agriculture Food and Drink Environment |
Description | COST ACTION CA22140 Improved Knowledge Transfer for Sustainable Insect Breeding (Insect-IMP) |
Geographic Reach | Europe |
Policy Influence Type | Participation in a guidance/advisory committee |
URL | https://e-services.cost.eu/action/CA22140/working-groups/view/1ee942a9-393b-63ee-bee8-0a58a9feac02 |
Description | International Partnerships fund |
Amount | £283,000 (GBP) |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Sector | Public |
Country | United Kingdom |
Start | 09/2022 |
End | 03/2023 |
Description | Investigating the role of sexual conflict in parasitoid-host eco-evolutionary dynamics |
Amount | £10,000 (GBP) |
Funding ID | IAP2-22-378 |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start | 09/2023 |
End | 03/2027 |
Description | Outreach 2023 grant |
Amount | £2,000 (GBP) |
Funding ID | OR23\1354 |
Organisation | British Ecological Society |
Sector | Charity/Non Profit |
Country | United Kingdom |
Start | 09/2023 |
End | 10/2024 |
Description | BBSRC International Partnership fund - Wageningnen University & Research |
Organisation | Wageningen University & Research |
Country | Netherlands |
Sector | Academic/University |
PI Contribution | Received funding through BBSRC International Partnerships fund to build a new partnership between Wageningen University and Stirling University to exploit our complementary expertise in environmentally sustainable crop protection research. Organised a workshop with UK (Stirling University and James Hutton Institute) and EU-based participants (WUR, EAWAG, Univ. Gothenberg) with the aim of developing schemes to (A) provide agriculture with a wider range of biocontrol agents with improved efficacy for diverse pests and cropping systems; (B) provide farmers with tools to manage threats posed by crop pests evolving resistance to current biocontrol agents. Hired a research assistant to help with the development of a novel database of the life-history characteristics of parasitoid wasp species, to assess factors influencing their success as biocontrol agents. |
Collaborator Contribution | Attended workshop at University of Stirling (Dec 2022) and presented research findings, workshopped follow up grant applications to apply for as a consortium, provided access to facilities and insects for molecular ecology/testing the evolution of resistance to biocontrol agents. |
Impact | Workshop - Sustainable futures for biocontrol-based crop protection |
Start Year | 2022 |
Description | EAWAG collaboration |
Organisation | Swiss Federal Institute of Aquatic Science and Technology |
Country | Switzerland |
Sector | Public |
PI Contribution | Discussion with postgraduate students about data analyses and planning follow up studies. |
Collaborator Contribution | Provided parasitoid wasps for experimental research, training in how to handle and rear the wasps, guidance on molecular techniques to use to answer questions of interest |
Impact | EAWAG invited seminar presentation This collaboration is not multidisciplinary. |
Start Year | 2021 |
Description | Bias in our publications discussion group |
Form Of Engagement Activity | A formal working group, expert panel or dialogue |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | On-going discussion group about how to identify patterns of gender bias in bibliometric datasets. Group consists of researchers from a range of backgrounds (life sciences, physical sciences, computer sciences, gender studies). Initial aim was to set up a panel discussion, but this has lead to ongoing monthly meetings where group members share their findings from their fields. The group is not putting together an opinion piece on the efficacy of different women in science schemes for increasing retention, wellbeing, productivity and success for women in science, based on bibliometrics. |
Year(s) Of Engagement Activity | 2021,2022 |
Description | Did Darwin Get it Wrong? |
Form Of Engagement Activity | A broadcast e.g. TV/radio/film/podcast (other than news/press) |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Media (as a channel to the public) |
Results and Impact | National Film and Television Graduate Showcase 2024: Did Darwin Get it Wrong? A film by Oliver Cummings Synopsis When Darwin published his famous theory, he allowed some good old-fashioned Victorian patriarchy influence his interpretation of nature, deeming the female role in sexual selection largely irrelevant. This is the story of why it took science 150 years to redress the balance. NFTS Crew Director/Producer/Sound Recordist - Oliver Cummins Cameras - Oliver Cummins, Sunshine Hsien-Yu Niu Production Manager - Teodora Petre Editor - James Jameson Foley Artist/Sound Designer/Dubbing Mixer - Alex Lunney Composer - Lucas Wide Colourist/Online Editor - Emmanuel Benjamin |
Year(s) Of Engagement Activity | 2024 |
URL | https://screeningroom.nfts.co.uk/graduate-showcase-2024/detail/videos/science-natural-history/video/... |
Description | EAWAG Zurich invited seminar |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Other audiences |
Results and Impact | Invited in-person seminar and lab visit to present and discuss past, present and future research. |
Year(s) Of Engagement Activity | 2021 |
Description | Early Career Researchers in Biocontrol international networking and fellowship writing workshop |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Postgraduate students |
Results and Impact | This event was part of the BBSRC International Partnership fund. The purpose was to connect early career researchers (PhD students and postdocs) from the University of Stirling and in Europe (Wageningen University, Netherlands & EAWAG, Switzerland) to build new international networks with their peers. On the trip ECRs engaged in a fellowship and grant writing workshop, PhD students worked on ideas that they had for follow-up projects after the end of their postgraduate studies. The group also provided information on a range of fellowships that the ECRs were eligible to apply for, and considered different funding options post-PhD. I organised travel and accommodation for the group and facilitated the workshops. |
Year(s) Of Engagement Activity | 2023 |
Description | Edinburgh Fringe Festival - Ugly Animals Preservation Society |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Public/other audiences |
Results and Impact | Invited to perform at the Edinburgh Fringe Festival by Simon Watt for the 'Ugly Animal Preservation Society' 10th anniversary. Performed a stand-up comedy set about the importance of parasitoid wasps. |
Year(s) Of Engagement Activity | 2022 |
URL | https://www.comedy.co.uk/fringe/2022/simon-watt/ |
Description | International day of women and girls in science - vlog/blog feature on website and social media |
Form Of Engagement Activity | Engagement focused website, blog or social media channel |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Undergraduate students |
Results and Impact | Interviewed by the Univerity of Stirling social media team for International women and girls in science day 2022. Video blog and online blog posted to social media channels and website https://blog.stir.ac.uk/international-women-in-science-day-becky-boulton/ |
Year(s) Of Engagement Activity | 2022 |
URL | https://twitter.com/StirUni/status/1492097414660034564?s=20&t=xwLTMZqPrEBk9Zz-rgHn6g |
Description | International workshop on resistance to biocontrol |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Industry/Business |
Results and Impact | For over half a century most crop protection has relied on chemical pesticides. Biological control represents an environmentally sustainable alternative to conventional chemical pesticides, minimising ecological damage and providing health benefits for consumers and farmers. This workshop brought researchers and stakeholders working across biocontrol systems together to explore ways to ensure biological control remains sustainable in the long-term by minimising the risk that hosts evolve resistance to biocontrol agents. I organised the workshop, which included 10 delegates from the Netherlands, Switzerland, Sweden, the UK (Stirling University and the James Hutton Institute). At the end of the workshop we discussed potential options for collaboration in the future including relelvant grants to be applied for. |
Year(s) Of Engagement Activity | 2022 |
Description | Stirling Science Festival - Albert Halls family day |
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 | Stand at Stirling Science festival (attended by over 800 individuals). Introduced children and adults to parasitoid wasps and their importance as biocontrol agents using a dissecting microscope with a tablet attached and an interactive farming game. |
Year(s) Of Engagement Activity | 2022 |
URL | https://stirlingevents.org/albert-halls-event/albert-halls-family-day/ |
Description | University of Exeter CEC seminar series |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Other audiences |
Results and Impact | Invited seminar at the University of Exeter about my past, present and future research. |
Year(s) Of Engagement Activity | 2021 |
Description | University of Stirling BES Seminar series |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Other audiences |
Results and Impact | Invited in-person seminar and lab visit to present and discuss past, present and future research. |
Year(s) Of Engagement Activity | 2022 |