The evolution of female mating systems: tracing the origins and tracking the consequences

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.

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.