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Alternative evolutionary outcomes following endosymbiont-mediated selection on male mating preference alleles
Antje Hundertmark1, Sara L Goodacre1, John F Y Brookfield1
1School of Life Sciences, University of Nottingham, University Park, Nottingham, UK.
Abstract:
In many arthropods, intracellular bacteria, such as those of the genus Wolbachia, may spread through host populations as a result of cytoplasmic incompatibility (CI). Here, there is sterility or reduced fertility in crosses between infected males and uninfected females. As the bacterium is maternally inherited, the reduced fertility of uninfected females increases the frequency of the infection. If the transmission fidelity of the bacterium is less than 100%, the bacterium cannot invade from a low frequency, but if its frequency exceeds a threshold, it increases to a high, stable, equilibrium frequency. We explore the expected evolutionary dynamics of mutant alleles that cause their male bearers to avoid mating with uninfected females. For alleles which create this avoidance behaviour conditional upon the male being infected, there is a wide zone of parameter space that allows the preference allele to drive Wolbachia from the population when it would otherwise stably persist. There is also a wide zone of parameter space that allows a joint stable equilibrium for the Wolbachia and a polymorphism for the preference allele. When the male's avoidance of uninfected females is unconditional, the preference allele's effect on Wolbachia frequency is reduced, but there is a narrow range of values for the transmission rate and CI fertility that allow an unconditional preference allele to drive Wolbachia from the population, in a process driven by positive linkage disequilibrium between Wolbachia and the preference allele. The possibility of the evolution of preference could hamper attempts to manipulate wild populations through Wolbachia introductions.
Insights
Male mating preferences can drive Wolbachia bacteria out of arthropod populations. This occurs when males avoid mating with uninfected females, potentially hindering bacterial control strategies.
Area of Science:
- Evolutionary biology
- Microbiology
- Genetics
Background:
- Wolbachia bacteria spread through arthropod populations via cytoplasmic incompatibility (CI), causing reduced fertility in crosses between infected males and uninfected females.
- Maternal inheritance of Wolbachia and CI create a threshold frequency for bacterial invasion and stable persistence in host populations.
Purpose of the Study:
- To investigate the evolutionary dynamics of male mating preference alleles that influence Wolbachia-driven CI.
- To determine conditions under which these preference alleles can eliminate or coexist with Wolbachia infections.
Main Methods:
- Mathematical modeling of allele frequency dynamics.
- Analysis of conditional and unconditional male mating preferences.
- Exploration of parameter space including transmission fidelity and CI fertility.
Main Results:
- Conditional preference alleles can drive Wolbachia to extinction or lead to a stable joint equilibrium with the bacteria.
- Unconditional preference alleles have a reduced effect but can still eliminate Wolbachia under specific transmission and fertility rates.
- Positive linkage disequilibrium can facilitate the spread of unconditional preference alleles.
Conclusions:
- The evolution of male mating preferences can significantly impact Wolbachia population dynamics.
- These preferences can potentially disrupt or alter strategies aimed at manipulating arthropod populations using Wolbachia.
- Understanding these evolutionary feedbacks is crucial for effective biocontrol applications.
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