Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds

Abstract

Appropriately timed integration of breeding into avian annual cycles is critical to both reproductive success and survival. The mechanisms by which birds regulate timing of breeding depend on environmental cue response systems that regulate both when birds do and do not breed. Despite there being multiple possible explanations for birds' abilities to time breeding appropriately in different environments, and for the distribution of different cue response system characteristics among taxa, many studies infer that adaptive specialization of cue response systems has occurred without explicitly considering the alternatives. In this paper, we make explicit three hypotheses concerning the timing of reproduction and distribution of cue response characteristics among taxa: adaptive specialization; conditional plasticity; and phylogenetic history. We emphasize in particular that although conditional plasticity built into avian cue response systems (e.g. differing rates of gonadal development and differing latencies until onset of photorefractoriness) may lead to maladaptive annual cycles in some novel circumstances, this plasticity also can lead to what appear to be adaptively specialized cue response systems if not viewed in a comparative context. We use a comparative approach to account for the distribution of one important feature of avian reproductive cue response systems, photorefractoriness. Analysis of the distribution within songbirds of one criterion for absolute photorefractoriness, the spontaneous regression of the gonads without any decline in photoperiod, reveals that a failure to display this trait probably represents an adaptive specialization to facilitate a flexible reproductive schedule. More finely resolved analysis of both criteria for absolute photorefractoriness (the second being total lack of a reproductive response even to constant light after gonadal regression has occurred) within the cardueline finches not only provides further confirmation of this interpretation, but also indicates that these two criteria for photorefractoriness can be, and have been, uncoupled in some taxa. We suggest that careful comparative studies at different phylogenetic scales will be extremely valuable for distinguishing between adaptive specialization and non-adaptive explanations, such as phylogenetic history as explanations of cue response traits in particular taxa. We also suggest that particular focus on taxa in which individuals may breed on very different photoperiods (latitudes or times of year) in different years should be particularly valuable in identifying the range of environmental conditions across which conditionally plastic cue responses can be adaptive.

Figure 1

Schematic illustrating conditional plasticity, whereby two birds with identical photoperiod response systems could exhibit different breeding schedules as a result of differing latitude. (a) At high latitudes, photophase increases more rapidly in spring, resulting in greater photoperiodic drive: gonads recrudesce more rapidly and refractoriness has an earlier onset. (b) Non-photic cues have reduced impact on reproductive flexibility (shaded area) because photoperiod drives the reproductive axis at near-maximal capacity. (c) At mid-latitudes photoperiodic drive is reduced: gonads recrudesce more slowly and refractoriness has a later onset. Non-photic cues can have larger impact on onset and offset of breeding.

Figure 2

Distribution of absolute refractoriness defined by criterion 1 (spontaneous regression of gonads on constant long days). Phylogeny adapted from Sibley & Ahlquist (1990), based on DNA–DNA hybridization. Higher-order taxa, common names of taxa and references in table 2.

Figure 3

Distribution of two criteria for absolute photorefractoriness among cardueline finches. (a) Criterion 1 is spontaneous gonadal regression while on constant long days. (b) Criterion 2 is unresponsiveness to long days (24 hour light in the extreme) during photorefractoriness. Common names of taxa and references in table 2. Phylogeny adapted from Marten & Johnson (1986), Badyaev (1997) and Arnaiz-Villena et al. (2001).