Epigenetics as an answer to Darwin's "special difficulty," Part 2: natural selection of metastable epialleles in honeybee castes.

Douglas M Ruden,Xiangyi Lu,Vincent E Sollars,Mark D Garfinkel,Marie-Claude Senut,Pablo E Cingolani,Arko Sen,Wen Qu,Luan Wang

doi:10.3389/fgene.2015.00060

Abstract

In a recent perspective in this journal, Herb (2014) discussed how epigenetics is a possible mechanism to circumvent Charles Darwin’s “special difficulty” in using natural selection to explain the existence of the sterile-fertile dimorphism in eusocial insects. Darwin’s classic book “On the Origin of Species by Means of Natural Selection” explains how natural selection of the fittest individuals in a population can allow a species to adapt to a novel or changing environment. However, in bees and other eusocial insects, such as ants and termites, there exist two or more castes of genetically similar females, from fertile queens to multiple sub-castes of sterile workers, with vastly different phenotypes, lifespans, and behaviors. This necessitates the selection of groups (or kin) rather than individuals in the evolution of honeybee hives, but group and kin selection theories of evolution are controversial and mechanistically uncertain. Also, group selection would seem to be prohibitively inefficient because the effective population size of a colony is reduced from thousands to a single breeding queen. In this follow-up perspective, we elaborate on possible mechanisms for how a combination of both epigenetics, specifically, the selection of metastable epialleles, and genetics, the selection of mutations generated by the selected metastable epialleles, allows for a combined means for selection amongst the fertile members of a species to increase colony fitness. This “intra-caste evolution” hypothesis is a variation of the epigenetic directed genetic error hypothesis, which proposes that selected metastable epialleles increase genetic variability by directing mutations specifically to the epialleles. Natural selection of random metastable epialleles followed by a second round of natural selection of random mutations generated by the metastable epialleles would allow a way around the small effective population size of eusocial insects.

Highlights

All of the groups that performed whole-genome shotgun bisulfite sequencing to map the 5mC distribution in honeybees found, at first impression paradoxically, that the low-CG content genes have much more DNA methylation than the high-CG content genes (Lyko et al, 2010; Zemach et al, 2010; Chen et al, 2011; Figure 1C)
EPIGENETIC DIRECTED GENETIC ERRORS IN NON-CG DINCULEOTIDES IN METASTABLE EPIALLELES In the epigenetic directed genetic error (EDGE) hypothesis, we propose that methylated cytosines are mutagenic in the 5mC sites and in the surrounding bases
We propose an intra-caste model of evolution that is based on selection of metastable epialleles in worker bees that runs parallel to the macro-evolution and group selection of DNA mutations

Summary

Introduction

All of the groups that performed whole-genome shotgun bisulfite sequencing to map the 5mC distribution in honeybees found, at first impression paradoxically, that the low-CG content genes have much more DNA methylation than the high-CG content genes (Lyko et al, 2010; Zemach et al, 2010; Chen et al, 2011; Figure 1C). We explore the possibility that metastable epiallele hyper-mutability, a key component of the EDGE hypothesis, is an emergent property of bimodal levels of DNA methylation in eusocial insects.

Results

Conclusion