THE INTERACTION OF BEHAVIORAL AND MORPHOLOGICAL CHANGE IN THE EVOLUTION OF A NOVEL LOCOMOTOR TYPE: "FLYING" FROGS.

"Flying" frogs have evolved independently several times among anurans. In all cases flyers are distinguished from their nonflying arboreal relatives by a unique set of morphological features and behavioral postures. Using both live animal field tests and wind tunnel models, this study examines the importance of this characteristic morphology and limb position on five aerial performance variables: horizontal traveling distance, minimum glide speed, maximum time aloft, maneuverability, and stability. Comparison of relative performance between a model frog with a generalized nonflying morphology and limb position and a model frog with flying morphology and limb position reveals that the morphological and positional features associated with "flying" actually decrease horizontal traveling distance but improve maneuverability. This finding suggests that maneuverability rather than horizontal travel may be the key performance parameter in the evolution of "flying" frogs. More generally, this study illustrates that (1) derived morphological and postural features do not necessarily change a suite of performance variables in the same way, and (2) the performance consequences of postural shifts are a function of morphology. These findings indicate that the potential complexity of morphological and behavioral interactions in the evolution of new adaptive types is much greater than previously considered.

EVALUATING A HYPOTHESIS ABOUT HETEROCHRONY: LARVAL LIFE-HISTORY TRAITS AND JUVENILE HIND-LIMB MORPHOLOGY IN HYLA CRUCIFER.

This paper reports the results of an investigation into whether selection on genetically based differences in the timing or rate of development (heterochrony) can give rise to nonadaptive morphological differences among individual frogs. We used a quantitative-genetics approach to examine the relationships among the life-history characters time to metamorphosis and larval-growth rate and a functionally significant morphological features, relative hind-limb length, in the spring peeper, Hyla crucifer. Time to metamorphosis and growth rate had low heritabilities in our population. Morphological traits had moderate heritabilities. There were positive genetic correlations between the life-history traits and the components of relative hind-limb length but no significant correlations with the shape variable itself. We used field observations of pond-drying time and experimental results of selection on growth rate to simulate the correlated responses of hind-limb shape to four reasonable selection regimes on the life-history traits. We found little evidence to suggest that relative hind-limb length would display much of a correlated response to such selection. The differences in relative hind-limb length seen among closely related species or among populations of a single species that appear to be unrelated to performance differences are not obviously explicable as neutral correlated responses to selection on larval traits.

A QUANTITATIVE-GENETIC ANALYSIS OF LARVAL LIFE-HISTORY TRAITS IN HYLA CRUCIFER.

We used a half-sib design to examine the genetic components of phenotypic variance in several life-history traits in Hyla crucifer. Egg viability, hatchling size, larval growth rate, length of larval period, and size at metamorphosis play critical roles in determining survivorship and are subject to persistent selection. Egg viability varied among families considerably, with most embryo mortality occurring between gastrulation and neurulation. Hatchling size was the only trait in which maternal effects were influential. Dominance genetic variance played the predominant role in determining phenotypic variance in hatchling size, growth rate, and length of larval period, accounting for, respectively, 70, 63, and 47% of the total variance. Size at metamorphosis displayed little dominance genetic variance and, unlike the other traits, displayed a high heritability. All additive genetic correlations between traits were positive. The directions of environmental correlations were the same as the directions of changes that have been induced in previous experimental work. The correlations due to dominance effects described a principal axis that independent ecological studies indicate to be directly correlated with fitness. These results agree with theoretical expectations for traits under consistent directional selection.

Ecological correlates of anuran exercise physiology.

Studies of exercise physiology of anuran amphibians have led to the suggestion that there is a dichotomy between species that depend upon movement to escape from predators and species that utilize static defenses. This generalization has been based upon a limited taxonomic survey and it contrasts with morphological, ecological, and behavioral studies that have revealed diverse and complex interrelationships among these features of anuran biology. We tested the hypothesis of a dichotomy of physiological types among anurans by measuring aerobic and anaerobic metabolism during maximum exercise for 17 species representing seven families and a variety of ecological types and locomotor modes. All degrees of dependence upon aerobic and anaerobic power input were found among the 17 species and the variation did not follow phylogenetic divisions. No single, simple prediction of the predominant source of power utilized for activity by the anurans we studied is possible. Predator avoidance behavior was not significantly correlated with the metabolic pattern. Predatory mode (active versus passive searchers) and mode of locomotion (non-jumpers versus jumpers) were correlated with dependence upon aerobic energy production and with each other. Reproductive behavior is probably another associated factor. The diversity of modes of power input among anurans is great and is intimately linked with numerous features of a species' biology. Single-factor explanations of this physiological characteristic are not appropriate.

Muscle activity at the ilio-sacral articulation of frogs.

Electromyographic recording indicates that the sequence of muscle firing around the ilio-sacral joint is similar for three species of frogs during locomotion, despite differences in gross morphology at the articulation. The ilio-sacral musculature is most active during the take-off phase of a jump, and there is a correlation between the degree of muscle activity and height of jump. This muscle activity is involved in aligning the center of mass of the frog with the direction of the propulsive force of the jump. The firing pattern of the ilio-sacral musculature is essentially similar during swimming and jumping, and suggests that differences in medium (water vs. air) are responsible for differences in propulsive thrust in the two types of locomotion.

Burrowing in frogs.

More than 95% of burrowing Anura dig hindfeet first into the soil, a pattern unique to frogs among terrestrial vertebrates. The postero-laterally placed hindlimbs and associated musculature of frogs are preadaptations for hindfeet digging. One fossorial, backwards burrower, Glyphoglossus molossus (Microhylidae), has morphological modifications of the hindlimb for positioning the spade-like metatarsal tubercle and for increasing the force of the lower leg during digging. In contrast, in the headfirst burrower Hemisus marmoratus (Ranidae) there is extensive reorganization of the pectoral-cranial morphology compared to that: of a non-burrowing confamilial species. A model links the shifts in the pectoral morphology in Hemisus marmoratus to specific action patterns of headfirst: burrowing. Finally, data on stomach contents, natural history and energy utilization of frog species are presented to demonstrate the interrelationships of distinct loco. motor patterns with specific feeding strategies.