PI Name: Thomas P. Coombs-Hahn Award Number: IOS-0744705 Proposal Title: Evolution of environmental cue response systems
Conditions on earth vary over time. How animals cope with this variation determines whether or not they can survive and reproduce successfully in particular environments. This project explores a key aspect of animals ability to survive and reproduce successfully in different environments: their ability to time reproduction appropriately as conditions change. Timing of reproduction is of the utmost importance because ill-timed attempts (when weather or food supply are not favorable, for instance) can be catastrophic. The project focuses on understanding how animals use information from the environment, so-called environmental cues such as seasonal changes in day-length, to time changes in physiology and behavior that are critical to survival and successful reproduction in changing environments. The project exploits natural variation in the breeding schedules of wild birds to determine whether different timing challenges presented by different environments (i.e., predictably or unpredictably changing food supply) require animals to possess specialized neuro-hormonal cue response mechanisms that are uniquely suited only to a limited set of environmental circumstances. Alternatively, more generalist solutions that work well under a variety of circumstances might prevail. The project is of fundamental interest in the field of environmental physiology, and is particularly timely because the results will provide a general conceptual basis for anticipating how animals adapted to different types of timing challenges (e.g., highly predictable or highly unpredictable variation in environmental conditions) are likely to differ in how they will be affected by human-induced modifications to the environment (e.g., climate and global warming). The project involves extensive training of young biologists, including members of under-represented groups, undergraduate students, masters and doctoral students, and postdoctoral trainees. It also involves extensive outreach beyond the academic setting, through public lectures, presentations in public schools, and web sites.
Conditions on earth vary in space and time, requiring animals to adjust their physiology, morphology and behavior in order to survive and reproduce successfully. These adjustments produces what are known as annual schedules of reproduction, migration, plumage or pelage replacement, hibernation, etc. Appropriate timing of these adjustments depends on environmental cues, such as the seasonal changes in day length, temperature, food supply, and social information. These cues provide both long- and short-term predictive information regarding impending changes in environmental conditions. In order to use these predictive cues, animals must possess mechanisms by which they can detect the cues, and then transduce the information from the cues into neural, neuro-hormonal and hormonal signals that orchestrate the annual schedule of changing physiology, morphology and behavior. This project focused on understanding between-species variation in how environmental cues are used to make these adjustments. Specifically, the study addressed the question of whether species coping with environments that differ in the predictability of changes in conditions have evolved adaptively specialized responses to environmental cues, or whether alternatively there exists a common set of widely shared cue response mechanisms that can produce appropriate annual schedules under diverse conditions. The study exploited the variation in temporal flexibility of temperate zone songbirds to address this question. This study demonstrated an interesting combination of widely shared "conditionally plastic" patterns and mechanisms of response to environmental cues and "adaptively specialized" patterns and mechanisms unique to a few species. All species studied, even those that can breed on both the shortest and longest days of the year, were "photoperiodic" in the sense that long days at least enhanced or accelerated reproductive development. However some species are "obligately" photoperiodic, requiring stimulation by relatively long days in order for other cues such as food or social factors to have augmenting effects. The most temporally flexible species – those that exploit resources that are particularly unpredictable in time and space – were much less dependent on a long day cue, and could enter full breeding condition even on very short days if other cues such as food and social factors were stimulatory. Most notably, these very flexible species have adaptively lost the ancestral trait of becoming "reproductively photorefractory," or unresponsive to the stimulatory effects of long days, permitting them to maintain reproductive competence if unpredictably favorable conditions for reproduction persist. This adaptive specialization enhancing flexibility of the annual schedule was correlated with unique features of the neuro-hormonal system in these species; the seasonal "switching off" of the Gonadotropin-releasing Hormone system of the brain that controls the seasonal termination of breeding in more strictly seasonal species was absent in these highly flexible species. This study also revealed a number of specific details about how flexible species adjust the scheduling of their annual cycles, and how flexible and less flexible species differ in regulating transitions from one stage of the annual cycle to the next. For instance, highly flexible species are exquisitely sensitive to changes in food supply, and to subtle cues from companions or mates. These short-term cues have dramatic effects on the scheduling of reproductive development, as well as the timing of nomadic migrations that allow them to cope effectively with unpredictable declines in food supply. Likewise, timing of plumage molt – a process that is critical to survival but conflicts with reproduction – was more sensitive to persistently elevated reproductive hormones in highly flexible species than in more rigidly seasonal ones. All of these results support the hypothesis that these very flexible species possess adaptively specialized patterns and mechanisms of response to environmental cues that enhance their ability to cope with unpredictability in the environment. In a broad sense, the results of this project provide some new perspectives on how different species are likely to be affected by environmental issues of current interest, such as global climate change. We are still a long way from being able to predict accurately which species are most likely to be affected negatively by rapid modifications of the environment. But this study is consistent with the idea that more flexible species, with highly plastic patterns of processing environmental cues, may be able to cope more effectively with a rapidly changing environment than would species that have evolved to rely very heavily on a single cue such as day length to set their annual schedules. Another important outcome of this project was that it provided numerous young scientists – including undergraduate students, masters students, doctoral students, and postdoctoral fellows – with professional development opportunities that enhanced their transitions into graduate school in biology, medical school, and veterinary school. Many of the trainees were young women, and several were individuals from under-represented groups, including Hispanic and African American women and men, and individuals who were the first in their families to have ever attended college.
