Abstract

Theory predicts that sexual reproduction promotes disease invasion by increasing the evolutionary potential of the parasite, whereas asexual reproduction tends to enhance establishment success and population growth rate. Gyrodactylid monogeneans are ubiquitous ectoparasites of teleost fish, and the evolutionary success of the specious Gyrodactylus genus is thought to be partly due to their use of various modes of reproduction. Gyrodactylus turnbulli is a natural parasite of the guppy (Poecilia reticulata), a small, tropical fish used as a model for behavioural, ecological and evolutionary studies. Using experimental infections and a recently developed microsatellite marker, we conclusively show that monogenean parasites reproduce sexually. Conservatively, we estimate that sexual recombination occurs and that between 3.7–10.9% of the parasites in our experimental crosses are hybrid genotypes with ancestors from different laboratory strains of G. turnbulli. We also provide evidence of hybrid vigour and/or inter-strain competition, which appeared to lead to a higher maximum parasite load in mixed infections. Finally, we demonstrate inbreeding avoidance for the first time in platyhelminths which may influence the distribution of parasites within a host and their subsequent exposure to the host's localized immune response. Combined reproductive modes and inbreeding avoidance may explain the extreme evolutionary diversification success of parasites such as Gyrodactylus, where host-parasite coevolution is punctuated by relatively frequent host switching.

Highlights

  • The widespread occurrence of sex is usually attributed to the fact that recombination generates new gene combinations, thereby increasing the rate of adaptive evolution whilst negating Muller’s ratchet and the associated irreversible accumulation of deleterious mutations [1]

  • Hybrid genotypes recovered at D14 from the Gt36Gt1 and Gt86Gt1 parasite lines, respectively, in Experiment 1

  • This study unambiguously demonstrates the occurrence of sexual recombination in a monogenean parasite, Gyrodactylus turnbulli, by making experimental crosses and using a microsatellite marker to identify sexually derived parasites

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Summary

Introduction

The widespread occurrence of sex is usually attributed to the fact that recombination generates new gene combinations, thereby increasing the rate of adaptive evolution whilst negating Muller’s ratchet and the associated irreversible accumulation of deleterious mutations [1]. The deleterious effects of inbreeding are predicted to be least noticeable in populations with a long history of inbreeding, as this tends to purge deleterious mutations in the population [3,4,5,6]. The beneficial effects of outcrossing are expected to be most pronounced in the most inbred populations [2]. This prediction is based on the assumption that in highly-inbred populations at least some loci will have been fixed for recessive deleterious alleles by drift, and that outcrossing will restore these loci to a heterozygous state [7]. The benefits of outcrossing and hybrid vigour tend to decline in subsequent generations due to the breakdown of co-adapted gene complexes and epistatic gene interactions [2,8]

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