Host-parasite coevolution and the role of sex and inbreeding

Overview

One of the fundamental questions in evolutionary biology is: why is sex the dominant mode of reproduction when it is so much costlier than reproducing asexually? One potential hypothesis is that the recombination associated with sexual reproduction generates genetic diversity and allows mothers to produce offspring that are resistant to rapidly and continuously evolving parasite populations. The Red Queen hypothesis predicts that hosts and parasites should continually change in response to one another but this requires variation on which fluctuating selection can act. Additionally, sex can also provide genetic benefits through intense sexual selection, where mothers mate with the fittest males. However, when inbreeding is common, the benefits of sex compared to asex could decline or even disappear, as recombination would generate less genetic diversity. This could be problematic, for example, when habitat fragmentation isolates populations and increases levels of inbreeding. Despite many years of theory, there are few conclusive experimental tests of these predictions.

The NERC-funded Stirling Outdoor Disease Experiment (SODE) provides an opportunity to test the relationships between host sex, sexual selection, inbreeding and host-parasite coevolution. SODE is an established long-term project where twenty replicate pond populations of the facultatively sexual freshwater crustacean Daphnia magna and its sterilising bacterial parasite Pasteuria ramosa have been maintained over multiple years. Each pond was initiated with the same suite of Daphnia genotypes and the same parasite population. Over the past four years, the populations have diverged, and the host populations have experienced different levels of inbreeding.

The student will conduct a series of integrated field, mesocosm (SODE) and laboratory investigations to dissect the implications of host sexual reproduction for (co)evolutionary change in both host and parasite populations.

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Image Captions

Fig.1 Aerial photograph of the NERC funded Stirling Outdoor Disease Experiment (SODE). Each pond contains replicate genotypes of Daphnia and Pasteuria (infected Daphnia on left; healthy on right).

Methodology

The student will: (1) map Daphnia reproductive mode and sex ratios, as well as disease prevalence from wild and experimental SODE pond populations over time; (2) quantify the role of sexual selection in maximizing the advantages of sex over asex using controlled laboratory and SODE-based experiments; and (3) dissect the role of host sex and inbreeding on the evolution of parasite traits, again using controlled laboratory and SODE-based experiments.

Project Timeline

Year 1

Year 1: Undertake literature search. Conduct SODE-based experiment to dissect various environmental drivers that could shape the likelihood and severity of infection within epidemics. Specifically, the student will create netted enclosures within each pond, sample asexually reproducing females, sexually reproducing females and male Daphnia, and then use established microsatellite markers to: (1) track host genotype abundance across an epidemic season; and (2) identify the inter-annual reproductive fitness of these genotypes by identifying the frequency of their descendants in the following season. By measuring other aspects of the phenotype (such as fecundity and mating success), the student will also estimate the genetic correlations between different traits, and between levels of expression for the same trait across years. The student will also collect Pasteuria parasite samples for subsequent study. This project will provide data for the first manuscript.

Year 2

Year 2: The student will further interrogate the microsatellite genotype data to test the effects of both inbreeding and sexual selection with respect to parasite resistance. They will establish the paternity of each daughter Daphnia genotype and assess the degree of skew in male reproductive success between clones and test for non-random paternity. Having established the potential for sexual selection in this system, they will test whether male reproductive success of each genotype covaries with the frequency of Pasteuria infection in that genotype. The student will also collect Pasteuria parasite samples from SODE and both host and parasite samples from an established wild population for subsequent study. Write second manuscript and present findings at an international conference.

Year 3

Year 3: Using the previously collected SODE and wild population samples collected from years 1 and 2, the student will test how host sex and inbreeding interact to affect the evolution of Pasteuria transmission and virulence, and any consequent coevolutionary responses in its Daphnia host. Write further manuscripts and present findings to both lay audiences and other researchers at conference. The project is funded for 3.5 years.

Year 3.5

Year 3.5: Write further manuscripts and present findings to both lay audiences and other researchers at conference. Finish thesis.

Training
& Skills

The student will receive extensive training on field techniques and experimental design in order to undertake the empirical component of the project.
They will also attend courses to learn statistical modelling in R, a code-based statistical package.

The student will learn microsatellite population genetic analyses from Prof Mable (University of Glasgow).

The student will receive training on public communication of science, media interaction, presenting to an academic audience and writing for both lay and academic audiences.

The student will thus be equipped with a suite of coding, analytical and communication skills that will make them employable both within academia and in non-academic sectors.

References & further reading

Auld et al. (2016) Proc. R. Soc. B 283: 20162226.
Gerber et al. (2018) Proc. R. Soc. B 285: 20172176.
Johnson et al., (2010) Heredity 104: 573-582.

See other papers on the Auld and Mable websites.

Further Information

Please contact Dr. Stuart Auld, s.k.auld@stir.ac.uk.

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