Sex-specific expression of circadian rhythms enables allochronic speciation

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 towards 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.