Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene

Abstract

The independent evolution of morphological similarities is widespread. For simple traits, such as overall body colour, repeated transitions by means of mutations in the same gene may be common. However, for more complex traits, the possible genetic paths may be more numerous; the molecular mechanisms underlying their independent origins and the extent to which they are constrained to follow certain genetic paths are largely unknown. Here we show that a male wing pigmentation pattern involved in courtship display has been gained and lost multiple times in a Drosophila clade. Each of the cases we have analysed (two gains and two losses) involved regulatory changes at the pleiotropic pigmentation gene yellow. Losses involved the parallel inactivation of the same cis-regulatory element (CRE), with changes at a few nucleotides sufficient to account for the functional divergence of one element between two sibling species. Surprisingly, two independent gains of wing spots resulted from the co-option of distinct ancestral CREs. These results demonstrate how the functional diversification of the modular CREs of pleiotropic genes contributes to evolutionary novelty and the independent evolution of morphological similarities.

Divergence of annual and perennial species in the Brassicaceae and the contribution of cis‐acting variation at FLC orthologues

“…This approach has proven effective in, for example, identifying the mechanisms and direction of evolution of wing pigmentation patterns in the Drosophila genus (Prud'homme et al . 2006; Arnoult et al . 2013).…”

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

“…These changes are mediated by the gain and loss of transcription factor binding sites in the cis-regulatory regions of these genes [5][6][7]. Changing the binding sites for patterning factors in cis-regulatory regions of more specialized effector genes is assumed to be less pleiotropic than changing the transcription factor genes themselves.…”

“…For specialists, studies of insect pigmentation have provided insight into diverse branches of biology, including ecology, development, genetics, and physiology. More recently, studies of insect pigmentation have taken center stage in the young field of evolutionary developmental biology, contributing to emerging principles such as the co-option of shared genetic circuitry for the evolution of novel traits (examples in butterfly wing patterns [1][2][3]) and the prevalence of cis-regulatory evolution in morphological diversification (examples in Drosophila pigmentation [4][5][6][7]). Insect pigmentation is a highly variable trait, with spectacular differences between species, between populations of the same species, and between individuals within a population.…”

Evolving enhancer-promoter interactions within the tinman complex of the flour beetle,Tribolium castaneum

“…For example, regulatory changes in pitx1 lead to a reduction in the pelvic fins of certain populations of stickleback fish (Shapiro et al, 2004). Moreover, regulatory changes in the yellow locus have been implicated in the diverse patterns of wing spots among divergent drosophilids (Prud'homme et al, 2006). Additionally, pre-existing enhancers are known to evolve through binding site turnover.…”