Abstract
The major transition to eusociality required the evolution of a switch to canalize development into either a reproductive or a helper, the nature of which is currently unknown. Following predictions from the ‘theory of facilitated variation’, we identify sex differentiation pathways as promising candidates because of their pre-adaptation to regulating development of complex phenotypes. We show that conserved core genes, including the juvenile hormone-sensitive master sex differentiation gene doublesex (dsx) and a krüppel homolog 2 (kr-h2) with putative regulatory function, exhibit both sex and morph-specific expression across life stages in the ant Cardiocondyla obscurior. We hypothesize that genes in the sex differentiation cascade evolved perception of alternative input signals for caste differentiation (i.e. environmental or genetic cues), and that their inherent switch-like and epistatic behavior facilitated signal transfer to downstream targets, thus allowing them to control differential development into morphological castes.
Highlights
The mechanisms underlying the evolution of phenotypic novelty are hotly debated [1,2,3,4]
Queens and workers produced from inter-population crosses were heterozygous for diagnostic microsatellite markers, whereas emerging winged and wingless males as well as one sex mosaic individual expressing both male and female characters exclusively carried the maternal alleles (S1 Table)
Together with the horned beetle data reviewed above, our study suggests that core components of the sex differentiation pathway such as dsx can produce evolutionary novelty by acting as a switch for nutrition and juvenile hormone (JH)-sensitive growth and development
Summary
The mechanisms underlying the evolution of phenotypic novelty are hotly debated [1,2,3,4]. A key prediction of the ‘theory of facilitated variation’ [5] is that regulation acts on evolutionarily conserved switch mechanisms, which modulate expression of target loci controlling development This process may facilitate large and complex evolutionary steps because it brings together new combinations of inputs (internal or external stimuli) and outputs (phenotypes) but does not rely on evolution of genes involved in the processes per se. It is likely that regulatory mechanisms controlling one set of polyphenism are pre-adapted to evolve control over newly evolving polyphenisms, for two reasons Such mechanisms’ pre-existing sensitivities to variable cues make it more likely that they will evolve the ability to perceive alternative gradients of novel cues, relative to constitutively expressed genes. Their downstream target genes already show inter-individual variability in expression, and the organism will already have evolved alternative responses to this variability
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