Effects of developmental and growth history on metamorphosis in the gray treefrog, Hyla versicolor (Amphibia, Anura).

In ecological models, the timing of amphibian metamorphosis is dependent upon rate of larval growth, e.g., tadpoles that experience a decrease in growth rate can initiate meta- morphosis early. Recent authors have suggested that this plasticity may be lost at some point during the larval period. We tested this hypothesis by exposing groups of tadpoles of the gray treefrog, Hyla versicolor, to different growth schedules. In endocrine models, metamorphosis is dependent on thyroxine levels and thyroxine is antagonized by prolactin (amphibian larval growth hormone), consistent with the idea that a rapidly growing tadpole can delay metamorphosis. Thus, we also manipulated the rate of development by supplementing or maintaining natural thyroxine levels for half of the tadpoles in each growth treatment. All tadpoles that received thyroxine supple- ments metamorphosed at the same time regardless of growth history. They also metamorphosed earlier than tadpoles not treated with thyroxine. Tadpoles not given thyroxine supplements meta- morphosed at different times: those growing rapidly during day 15-34 metamorphosed earlier than tadpoles growing slowly. Growth rate before day 15 and after day 34 had no effect on meta- morphic timing. The difference in larval period between these rapidly growing tadpoles and their sisters given thyroxine treatments was less than the same comparison for tadpoles that grew slowly during the same period. This apparent prolactin/thyroxine antagonism did not exist after day 34. These results are consistent with the hypothesis of a loss of plasticity in metamorphic timing. J. Exp. Zool. 283:522n530, 1999. © 1999 Wiley-Liss, Inc. Given the importance of phenotypic plasticity as an adaptation to variable environments (Brad- shaw, '65; Levins, '68; Via, '87; Stearns, '89), it seems critical to uncover the mechanisms by which adaptive plasticity is controlled and lim- ited (Newman, '92). For example, the larval stage of most amphibians appears to be an opportunity to take advantage of transient growth opportuni- ties in ephemeral, productive habitats (Wassersug, '75; Wilbur, '80; Newman, '94). Because metamor- phosis represents an escape from these habitats, amphibians should initiate metamorphosis when- ever conditions become too hostile (e.g., pond-dry- ing). However, amphibians (especially tadpoles) commonly become trapped (and die) in the larval habitat before metamorphosis is possible (Wilbur, '80; Newman, '92). Metamorphosis in these animals is thought to represent a switchpoint during the life cycle that is designed to maximize the growth-to-mortality risk ratio in both the larval and adult environ- ments (Werner and Gilliam, '84; Werner, '86; Rowe and Ludwig, '91). Because the larval environment is often highly variable (e.g., pond-drying or ar- rival of predators is unpredictable), a larva that maintains a plastic response in timing of and/or size at metamorphosis may have higher fitness than one with fixed metamorphic parameters. Wilbur and Collins ('73) hypothesized that am- phibian larvae respond adaptively to resource variation by initiating metamorphosis when a larva experiences a decrease in growth. This re- sponse to a deteriorating environment (e.g., in- creasing density of competitors, presence of predators) is suggested to occur between a mini- mal size required to initiate metamorphosis and a maximal size when metamorphosis is obligatory. There is abundant evidence that larval growth history has significant effects on timing of meta- morphosis (Collins, '79; Semlitsch and Caldwell, '82; Semlitsch and Gibbons, '85; Alford and Har- ris, '88; Newman, '89; Skelly and Werner, '90;