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

Philosophical Transactions of the Royal Society B: Biological Sciences, Jan 2008

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.

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

Thomas P Hahn Scott A MacDougall-Shackleton phylogenetic history in the reproductive cue response Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here - Email alerting service To subscribe to Phil. Trans. R. Soc. B go to: http://rstb.royalsocietypublishing.org/subscriptions Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds 1University of California Davis, Davis, CA 95616, USA 2University of Western Ontario, 1151 Richmond Street, Suite 2, London, Ontario, Canada N6A 5B8 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. 1. INTRODUCTION: TIMING OF BREEDING AND FIT TO DIFFERENT ENVIRONMENTS A basic goal in biology is to understand how organisms come to be well suited to their environments ( Fretwell 1972). From a fitness standpoint, the choice of when to breed is a key indicator of being well suited to an environment, since timing of breeding affects both the likelihood of producing high-quality offspring and the probability of adult survival (Drent & Daan 1980; Farner et al. 1983; Svensson 1997; McNamara et al. 2004; Komdeur & Daan 2005; Verhulst & Nilsson 2008). In environments where conditions vary in space * Author and address for correspondence: Section of Neurobiology, Physiology and Behavior, University of California Davis, Davis, CA 95616, USA (). and time (i.e. most environments), the reproductive schedule should track changes in ultimate environmental factors (e.g. food supply, weather) that affect reproductive success (Baker 1938; Perrins 1970). Consequently, selection should favour individuals that possess mechanisms permitting them to detect and respond to proximate cues that predict impending relevant changes in the environment (Baker 1938). Processing of such cues is achieved by the neuroendocrine system, which transduces information from both external cues (e.g. changing day length, rainfall, food supply) and internal processes (e.g. the readout from circannual clocks and modulation, if any, of responsiveness to environmental cues) into neuroendocrine signals that regulate changes in reproductive physiology, morphology and behaviour (e.g. Follett 1984; Ball 1993). Appropriate timing of reproduction in a particular environm (...truncated)


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Thomas P Hahn, Scott A MacDougall-Shackleton. Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds, Philosophical Transactions of the Royal Society B: Biological Sciences, 2008, pp. 267-286, 363/1490, DOI: 10.1098/rstb.2007.2139