Solar noon and tactile cues synergistically regulate clutch size: a new approach to investigations of avian life‐history theory

Life-history theory is central to our understanding of the evolutionary processes that drive adaptation. According to life-history theory, a trade-off between reproduction and survival means that organisms cannot maximize both at the same time (Gadgil & Bossert 1970, Charnov & Krebs 1974, Stearns 1976, 1989, Reznick 1985, Morris 1986). As Reznick (1985) stated while reviewing the costs of reproduction, ‘To be the best in all possible worlds is not biologically possible; to be well adapted to even one world requires compromise.’ Throughout the progression of thought in life-history theory, clutch size has been a trait of primary interest. For over half a century, it has been argued that diverse selection pressures operate on clutch size in birds (Ricklefs 2000) so as to optimize it, although the relative importance of each pressure remains unclear. A few examples of competing selection pressures on clutch size include the trade-offs between clutch size and number of clutches in a given year, clutch size and parental care, clutch size and access to food resources, clutch size and parental age, and the list goes on. A vast body of literature demonstrates the extent of these trade-offs and their importance in understanding emergent avian lifehistory patterns, yet we still do not understand how birds regulate or determine clutch size. Although avian clutch size often varies systematically and in predictable ways, we cannot adequately explain the emergent patterns. While investigations have explored possible roles of predation, food availability and seasonality (e.g. Beukeboom et al. 1988, Hochachka 1990, Crick et al. 1993) on variation in clutch size, additional insights may be found by asking how (mechanistically) clutch size is determined, rather than why (evolutionarily). Such a shift in question might change our perception of which traits selection might be acting upon to optimize clutch size. A paper by Sacha Haywood in this issue of Ibis brings us closer to resolving a fundamental problem in identifying the proximate selection pressures regulating clutch size. Haywood’s egg removal experiments with Common Swifts Apus apus nicely demonstrate that the trait (or suite of traits) under selection is not the number of eggs in a clutch, an ordinal trait measured quantitatively, but rather the physiological mechanisms controlling the endpoint of the laying sequence. Haywood presents evidence that there is a specific point in time, approximately solar noon on the day the first egg is laid, that plays a decisive role in determining how many subsequent eggs will be produced (Haywood 2013). Haywood builds his argument in two parts. First he explores the possibility that the tactile cue that stops the production of yolky follicles is invariant in its timing. In other words, the production of yolky follicles is halted by the stimulus of the brood patch coming in contact with the first egg laid. Invariance in the timing of this tactile cue means that a second mechanism must come into play to account for the observed variability in egg production. Second, he postulates a role for an internal circadian clock that might govern the ability of ovarian tissue to receive and respond to hormone fluxes, thereby allowing for temporal plasticity in follicular development and eventual disruption. In the case of the Common Swift, this competency to receive the hormonal signal develops over a period of 3–6 h before solar noon on the day the first egg is laid, at which point it becomes fully functional. With these two mechanisms, Haywood’s model accounts for variability in clutch size in a species that would otherwise seem to be physiologically constrained to a predetermined number of eggs. A key implication of Haywood’s findings is that the focal point of life-history theory with regard to clutch size might actually be a set of physiological processes and their underlying gene regulation, rather than a single quantitative characteristic (i.e. number of eggs produced). A strong argument for considering physiological processes as the target of selection that subsequently drives life-history trade-offs was outlined by Sinervo and Svensson (1998). Haywood’s study fits this paradigm shift in that it forces us to view clutch size, a common life-history variable, not as a single quantitative trait under selection pressure but rather as the product of several intersecting endocrine feedback loops. Furthermore, his experimental results set the stage for clarification of the differentiation between determinate layers with invariant clutch size and indeterminate layers (variable clutch size). *Corresponding author. Email: mav11@psu.edu