Evolution of environmental cue response mechanisms: Adaptive variation in photorefractoriness

Appropriate timing of transitions between annual cycle stages (reproduction, plumage molt, migration) is critical to fitness for birds living in temporally varying environments. Environmental cue response systems permit birds to orchestrate these transitions. This paper focuses on how photorefractoriness and one neuroendocrine correlate of it (GnRH system plasticity) have evolved to permit appropriate timing of the transition from breeding to plumage molt. Photorefractoriness is defined by two criteria. Criterion 1: photoinduced gonadal regression occurs without any decline in photoperiod. Criterion 2: photoinduced gonadal regression cannot be reversed by increased photoperiod, even continuous light. Through a comparative approach we show that: (1) Loss of Refractoriness Criterion 1 and of GnRH system down-regulation appear to represent adaptive specializations favoring highly temporally flexible or continuous breeding, (2) Refractoriness Criteria 1 and 2 are not always concordant, and Criterion 2 in particular is not well-correlated with degree of temporal reproductive flexibility, (3) occurrence of some cue response traits are better-explained by phylogenetic relationships among taxa than by current reproductive schedules (seasonal, flexible, opportunistic), (4) substantial temporal flexibility can be achieved in a variety of ways besides adaptive modifications of refractoriness, such as relaxation of long-day requirements for reproductive development, and enhancement of non-photic cue responsiveness. These comparisons also highlight fundamental similarities between some of the most opportunistic species and seasonal breeders, such as an autumn reproductive hiatus during molt. Even in the face of substantial environmental unpredictability, selection may often strongly favor regular scheduling of particularly critical life cycle stages such as plumage molt.