Abstract

Parasite‐mediated selection is one of the main drivers of genetic variation in natural populations. The persistence of long‐term self‐fertilization, however, challenges the notion that low genetic variation and inbreeding compromise the host's ability to respond to pathogens. DNA methylation represents a potential mechanism for generating additional adaptive variation under low genetic diversity. We compared genetic diversity (microsatellites and AFLPs), variation in DNA methylation (MS‐AFLPs), and parasite loads in three populations of Kryptolebias hermaphroditus, a predomintanly self‐fertilizing fish, to analyze the potential adaptive value of DNA methylation in relation to genetic diversity and parasite loads. We found strong genetic population structuring, as well as differences in parasite loads and methylation levels among sampling sites and selfing lineages. Globally, the interaction between parasites and inbreeding with selfing lineages influenced DNA methylation, but parasites seemed more important in determining methylation levels at the local scale.

Highlights

  • Organisms with mixed‐mating reproduction can benefit from the advantages of both biparental and uniparental reproduction: outcrossing gener‐ ates genetic variability and adaptability potential, while selfing en‐ sures reproduction without partners (Jarne and Chalesworth 1993), and reproductive assurance (Darwin, 1876) gives self‐reproducing individuals an advantage when colonizing new environments (Baker, 1955)

  • Our results did not indicate significant differences in genome‐wide DNA methylation variation between selfed and out‐ crossed individuals, and our models only identified inbreeding status significantly re‐ lated to DNA methylation via its interaction with selfing lineage and parasites

  • Higher vari‐ ation in DNA methylation has been reported for clonal and inbred individuals (Liebl et al, 2013; Massicotte & Angers, 2012; Nakamura & Hosaka, 2010; Richards et al, 2012; Veerger et al, 2012) and has been interpreted as an adaptive mechanism to compensate for low genetic variation (Schrey et al, 2012), or as a potential consequence of inbreeding responsi‐ ble, at least in part, for inbreeding depression (Nakamura & Hosaka, 2010; Vergeer et al, 2012)

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Summary

| INTRODUCTION

Organisms with mixed‐mating reproduction (alternating between self‐fertilization and outcrossing) can benefit from the advantages of both biparental and uniparental reproduction: outcrossing gener‐ ates genetic variability and adaptability potential, while selfing en‐ sures reproduction without partners (Jarne and Chalesworth 1993), and reproductive assurance (Darwin, 1876) gives self‐reproducing individuals an advantage when colonizing new environments (Baker, 1955). The Red Queen hypothesis (Bell, 1982; Van Valen, 1973) is often invoked to explain the occurrence of sexual reproduction in face of the advantages of asexual reproduction (Blirt & Bell, 1987; Lively, 1987; Lively & Morran, 2014) According to this hypothesis, the more genetically diverse offspring of sexually reproducing individ‐ uals provide a “moving target” to parasites, making it more difficult for them to adapt compared to the “more static” offspring of asex‐ ual/uniparental individuals (Maynard Smith 1978; Hamilton, 1980; Lively, Craddock, & Vrijenhoek, 1990;). Given the relationship between genetic background and DNA methylation levels, we expected dif‐ ferent patterns of variation in DNA methylation across selfing lines and predicted higher levels of DNA methylation in relation to in‐ breeding and parasite loads, if methylation played an adaptive role, potentially related to pathogen infection, in K. hermaphroditus

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| DISCUSSION
Findings
ETHICAL APPROVAL
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