Sex-specific expression of circadian rhythms enables allochronic speciation

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Abstract Noctuid moths provide prime examples of species in various stages of allochronic speciation, where reproductive barriers are mediated by genetic divergence in daily or seasonal timing. Theory indicates that allochronic divergence might be one of the most plausible mechanisms of adaptive speciation, especially when timing is subject to divergent ecological selection. Here, we show that the validity of this theoretical expectation is entirely contingent on species characteristics of the mating system. Our analysis focuses on the moth Spodoptera frugiperda (Lepidoptera, Noctuidae), which occurs as two strains that differ in circadian reproductive activity. Unlike in generic models of assortative mating, where chronotypes diverge under mild assumptions, individual-based evolutionary simulations of the mating system and life cycle of S. frugiperda fail to recover allochronic diversification, even under conditions highly conducive to speciation. Instead, we observe that both chronotypes advance their activity schedule toward the early night, resulting in a rapid loss of allochronic variation. This outcome is caused by the fact that mating in S. frugiperda takes considerable time and potential mates are encountered sequentially, so that early males enjoy a systematic advantage. The undermining effect of male mate competition can be overcome when circadian genes evolve sex-specific expression, enabling early and late chronotypes to be maintained or even to diversify in sympatry. These results give new significance to sex differences in biological rhythms and suggest that species characteristics of the mating system and genetic architecture are key to understanding the scope for allochronic speciation across diverse species exhibiting variation in timing.