Phenotypic plasticity in the monoclonal marbled crayfish is associated with very low genetic diversity but pronounced epigenetic diversity

Abstract

Abstract Clonal organisms are particularly useful to investigate the contribution of epigenetics to phenotypic plasticity, because confounding effects of genetic variation are negligible. In the last decade, the apomictic parthenogenetic marbled crayfish, Procambarus virginalis, has been developed as a model to investigate the relationships between phenotypic plasticity and genetic and epigenetic diversity in detail. This crayfish originated about 30 years ago by autotriploidy from a single slough crayfish Procambarus fallax. As the result of human releases and active spreading, marbled crayfish has established numerous populations in very diverse habitats in 22 countries from the tropics to cold temperate regions. Studies in the laboratory and field revealed considerable plasticity in coloration, spination, morphometric parameters, growth, food preference, population structure, trophic position, and niche width. Illumina and PacBio whole-genome sequencing of marbled crayfish from representatives of 19 populations in Europe and Madagascar demonstrated extremely low genetic diversity within and among populations, indicating that the observed phenotypic diversity and ability to live in strikingly different environments are not due to adaptation by selection on genetic variation. In contrast, considerable differences were found between populations in the DNA methylation patterns of hundreds of genes, suggesting that the environmentally induced phenotypic plasticity is mediated by epigenetic mechanisms and corresponding changes in gene expression. Specific DNA methylation fingerprints persisted in local populations over successive years indicating the existence of epigenetic ecotypes, but there is presently no information as to whether these epigenetic signatures are transgenerationally inherited or established anew in each generation and whether the recorded phenotypic plasticity is adaptive or nonadaptive.