Epigenetics and locust life phase transitions

Abstract

Insects are one of the most successful classes on Earth, reflected in an enormous species richness and diversity. Arguably, this success is partly due to the high degree to which polyphenism, where one genotype gives rise to more than one phenotype, is exploited by many of its species. In social insects, for instance, larval diet influences the development into distinct castes; and locust polyphenism has tricked researchers for years into believing that the drastically different solitarious and gregarious phases might be different species. Solitarious locusts behave much as common grasshoppers. However, they are notorious for forming vast, devastating swarms upon crowding. These gregarious animals are shorter lived, less fecund and transmit their phase characteristics to their offspring. The behavioural gregarisation occurs within hours, yet the full display of gregarious characters takes several generations, as does the reversal to the solitarious phase. Hormones, neuropeptides and neurotransmitters influence some of the phase traits; however, none of the suggested mechanisms can account for all the observed differences, notably imprinting effects on longevity and fecundity. This is why, more recently, epigenetics has caught the interest of the polyphenism field. Accumulating evidence points towards a role for epigenetic regulation in locust phase polyphenism. This is corroborated in the economically important locust species Locusta migratoria and Schistocerca gregaria. Here, we review the key elements involved in phase transition in locusts and possible epigenetic regulation. We discuss the relative role of DNA methylation, histone modification and small RNA molecules, and suggest future research directions. KEY WORDS: Locust phase, Polyphenism, Locust swarming, Locusta migratoria, Schistocerca gregaria, Apis mellifera, Invertebrate, DNA methylation, Histone modification, Methylome IntroductionThe term epigenetics tends to take a variety of meanings (Haig, 2004;Jablonka and Lamb, 2002). In its narrow sense, it can be defined as 'meiotically and mitotically heritable changes in gene expression, not based on DNA sequence alterations ' (Riggs et al., 1996). In a broader sense, it can also be interpreted as 'modifications of chromosome structure ' (Bird, 2007). Independent of the interpretation, however, epigenetics did not receive much attention in insect research until recent years.The most prominent epigenetic mechanisms, namely (1) methylation of cytosine in DNA, (2) modifications of histone proteins and (3) nucleosome positioning and regulation by noncoding RNA, were only rarely the focus of the entomology field. This may have been due to the general low, often almost undetectable, levels of methylation in insects and other invertebrates REVIEW Functional Genomics and Proteomics Lab, KU Leuven, Naamsestraat 59, bus 2465, B-3000 Leuven, Belgium.*Author for correspondence (Liliane.Schoofs@bio.kuleuven.be) (Glastad et al., 2011), including the prime model organisms Drosophila melanogaster and Caenorhabdi...

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