Phenotypic Plasticity in Drosophila Pigmentation Caused by Temperature Sensitivity of a Chromatin Regulator Network

Abstract

Phenotypic plasticity is the ability of a genotype to produce contrasting phenotypes in different environments. Although many examples have been described, the responsible mechanisms are poorly understood. In particular, it is not clear how phenotypic plasticity is related to buffering, the maintenance of a constant phenotype against genetic or environmental variation. We investigate here the genetic basis of a particularly well described plastic phenotype: the abdominal pigmentation in female Drosophila melanogaster. Cold temperature induces a dark pigmentation, in particular in posterior segments, while higher temperature has the opposite effect. We show that the homeotic gene Abdominal-B (Abd-B) has a major role in the plasticity of pigmentation in the abdomen. Abd-B plays opposite roles on melanin production through the regulation of several pigmentation enzymes. This makes the control of pigmentation very unstable in the posterior abdomen, and we show that the relative spatio-temporal expression of limiting pigmentation enzymes in this region of the body is thermosensitive. Temperature acts on melanin production by modulating a chromatin regulator network, interacting genetically with the transcription factor bric-à-brac (bab), a target of Abd-B and Hsp83, encoding the chaperone Hsp90. Genetic disruption of this chromatin regulator network increases the effect of temperature and the instability of the pigmentation pattern in the posterior abdomen. Colocalizations on polytene chromosomes suggest that BAB and these chromatin regulators cooperate in the regulation of many targets, including several pigmentation enzymes. We show that they are also involved in sex comb development in males and that genetic destabilization of this network is also strongly modulated by temperature for this phenotype. Thus, we propose that phenotypic plasticity of pigmentation is a side effect reflecting a global impact of temperature on epigenetic mechanisms. Furthermore, the thermosensitivity of this network may be related to the high evolvability of several secondary sexual characters in the genus Drosophila.

yellow and ebony Are the Responsible Genes for the Larval Color Mutants of the Silkworm Bombyx mori

“…Mutations in the yellow gene produce an altered form of melanin, which results in the light ''Yellow'' coloration instead of the normal black coloration (Geyer et al 1986;Wright 1987;Wittkopp et al 2002a). Yellow protein may act in the melanin-synthesis pathway downstream from dopa and/or dopamine (Gibert et al 2007), although the precise function of Yellow remains unclear (Drapeau 2003;Gibert et al 2007).…”

Development and evolution of insect pigmentation: Genetic mechanisms and the potential consequences of pleiotropy

“…Geneby-environment interactions -an important, yet under-studied determinant of complex traits -can also be examined in this system: developmental plasticity for insect pigmentation is common (e.g. [7,10]), and some mechanisms by which environmental cues affect pigmentation have been identified [96,97].…”

Natural Variation of ebony Gene Controlling Thoracic Pigmentation in Drosophila melanogaster

“…The trident pattern shaped by dark pigmentation clearly appears in TW1 but not in Mel6. We checked the phenotype at three different temperatures-18°, 20°, and 25°-since temperature is known to affect the intensity of pigmentation (David et al 1985;Moreteau et al 1995;Gibert et al 2000Gibert et al , 2004Gibert et al , 2007Munjal et al 1997). The pigmentation of the TW1 line darkens when reared in lower temperatures, but no obvious trident shape appeared in Mel6 in the temperature range we tested (data not shown).…”