Tetrapod limbs have been used as a model system to investigate how selective pressures and constraints shape morphological evolution. Anurans have had many independent transitions to various ...microhabitats, allowing us to dissect how these factors influence limb morphology. Furthermore, anurans provide a unique system to test the generality of developmental constraints proposed in mammals, namely that later-developing limb bones are under less constraint and show more variation. We used microcomputed tomography scans of 236 species from 52 of 55 families, geometric morphometrics, and modern phylogenetic comparative methods to examine how limb bones are related to microhabitat, phylogeny, allometry, and developmental timing. Although there was significant phylogenetic signal, anuran limb shape showed a relationship with microhabitat and to a lesser extent, body size. We found that distal bones had higher evolutionary rates than proximal bones, providing evidence that developmental constraints are reduced in later-developing bones. Distal bones also showed increased selection related to allometry and microhabitat, providing an additional explanation for higher evolutionary rates. By looking at the evolution of limb shape across a diverse clade, we demonstrated that multiple factors have shaped anuran limbs and that greater evolutionary lability in later-developing limb bones is likely a general trend among tetrapods.
Surprisingly, little is known about body‐size evolution within the most diverse amphibian order, anurans (frogs and toads), despite known effects of body size on the physiological, ecological and ...life‐history traits of animals more generally. Here, we examined anuran body‐size evolution among 2,434 species with over 200 million years of shared evolutionary history. We found clade‐specific evolutionary shifts to new body‐size optima along with numerous independent transitions to gigantic and miniature body sizes, despite the upper limits of anuran body size remaining quite consistent throughout the fossil record. We found a weak, positive correlation between a species’ body size and maximum latitude and elevation, including a dearth of small species at higher elevations and broader latitudinal and elevational ranges in larger anurans. Although we found modest differences in mean anuran body size among microhabitats, there was extensive overlap in the range of body sizes across microhabitats. Finally, we found that larger anurans are more likely to consume vertebrate prey than smaller anurans are and that species with a free‐swimming larval phase during development are larger on average than those in which development into a froglet occurs within the egg. Overall, anuran body size does not conform to geographic and ecological patterns observed in other tetrapods but is perhaps more notable for variation in body size within geographic regions, ecologies and life histories. Here, we document this variation and propose target clades for detailed studies aimed at disentangling how and why variation in body size was generated and is maintained in anurans.
Shifts in body size evolution detected among 2,434 anuran species. Branches within the phylogeny are coloured based on estimated shifts in body size evolution. The estimated theta (evolutionary optima) for each bayou regime is listed on the bottom bar and the posterior probability of each shift is indicated by the size of the coloured circle. Maximum body size of each species is represented by the length of the bars on the perimeter of the tree. Miniature (<16 mm, red) and gigantic (>127 mm, blue) species’ bars are coloured. In clockwise order, anuran photos from select families within estimated shifts in body size evolution—eleutherodactylid (Eleutherodactylus portoricensis) credit: Alberto Lopez; brachycephalid (Brachycephalus ephippium) credit: C. Guilherme Becker; myobatrachid (Pseudophryne coriacea) credit: Rayna C. Bell; rhacophorid (Chiromantis rufescens) credit: Christian Irian; ranid (Amnirana albolabris), conrauid (Conraua crassipes), and bufonid (Nectophryne batesii) credit: Bryan Stuart; dendrobatid (Ranitomeya sirensis), centrolenid (Teratohyla midas) and leptodactylid (Lithodytes lineatus) credit: Ivan Prates.
Synopsis
Many anuran amphibians (frogs and toads) rely on aquatic habitats during their larval stage. The quality of this environment can significantly impact lifetime fitness and population ...dynamics. Over 450 studies have been published on environmental impacts on anuran developmental plasticity, yet we lack a synthesis of these effects across different environments. We conducted a meta-analysis and used a comparative approach to understand whether developmental plasticity in response to different larval environments produces predictable changes in metamorphic phenotypes. We analyzed data from 124 studies spanning 80 anuran species and six larval environments and showed that intraspecific variation in mass at metamorphosis and the duration of the larval period is partly explained by the type of environment experienced during the larval period. Changes in larval environments tended to reduce mass at metamorphosis relative to control conditions, with the degree of change depending on the identity and severity of environmental change. Higher temperatures and lower water levels shortened the duration of the larval period, whereas less food and higher densities increased the duration of the larval period. Phylogenetic relationships among species were not associated with interspecific variation in mass at metamorphosis plasticity or duration of the larval period plasticity. Our results provide a foundation for future studies on developmental plasticity, especially in response to global changes. This study provides motivation for additional work that links developmental plasticity with fitness consequences within and across life stages, as well as how the outcomes described here are altered in compounding environments.
Lay Summary
We conducted a meta-analysis to identify how six different environments affect mass at metamorphosis and time to metamorphosis in larval anurans. We find that some, but not all, environmental conditions triggered predictable changes in size and timing of metamorphosis, and phylogenetic relatedness rarely explains developmental plasticity variation among species.
Frog larvae (tadpoles) undergo many physiological, morphological and behavioral transformations throughout development before metamorphosing into their adult form. The surface tension of water ...prevents small tadpoles from breaching the surface to breathe air (including those of Xenopus laevis), forcing them to acquire air using a form of breathing called bubble sucking. With growth, tadpoles typically make a behavioral/biomechanical transition from bubble sucking to breaching. Xenopus laevis tadpoles have also been shown to transition physiologically from conforming passively to ambient oxygen levels to actively regulating their blood oxygen. However, it is unknown whether these mechanical and physiological breathing transitions are temporally or functionally linked, or how both transitions relate to lung maturation and gas exchange competency. If these transitions are linked, it could mean that one biomechanical breathing mode (breaching) is more physiologically proficient at acquiring gaseous oxygen than the other. Here, we describe the mechanics and development of air breathing and the ontogeny of lung morphology in X. laevis throughout the larval stage and examine our findings considering previous physiological work. We found that the transitions from bubble sucking to breaching and from oxygen conforming to oxygen regulation co-occur in X. laevis tadpoles at the same larval stage (Nieuwkoop-Faber stages 53-56 and 54-57, respectively), but that the lungs do not increase significantly in vascularization until metamorphosis, suggesting that lung maturation, alone, is not sufficient to account for increased pulmonary capacity earlier in development. Although breach breathing may confer a respiratory advantage, we remain unaware of a mechanistic explanation to account for this possibility. At present, the transition from bubble sucking to breaching appears simply to be a consequence of growth. Finally, we consider our results in the context of comparative air-breathing mechanics across vertebrates.
Anurans (frogs and toads) have a unique pelvic and hind limb skeleton among tetrapods. Although their distinct body plan is primarily associated with saltation, anuran species vary in their primary ...locomotor mode (e.g., walkers, hoppers, jumpers, and swimmers) and are found in a wide array of microhabitats (e.g., burrowing, terrestrial, arboreal, and aquatic) with varying functional demands. Given their largely conserved body plan, morphological adaptation to these diverse niches likely results from more fine-scale morphological change. Our study determines how shape differences in Anura's unique pelvic and hind limb skeletal structures vary with microhabitat, locomotor mode, and jumping ability. Using microCT scans of preserved specimens from museum collections, we added 3D landmarks to the pelvic and hind limb skeleton of 230 anuran species. In addition, we compiled microhabitat and locomotor data from the literature for these species that span 52 of the 55 families of frogs and ∼210 million years of anuran evolution. Using this robust dataset, we examine the relationship between pelvic and hind limb morphology and phylogenetic history, allometry, microhabitat, and locomotor mode. We find pelvic and hind limb changes associated with shifts in microhabitat ("ecomorphs") and locomotor mode ("locomorphs") and directly relate those morphological changes to the jumping ability of individual species. We also reveal how individual bones vary in evolutionary rate and their association with phylogeny, body size, microhabitat, and locomotor mode. Our findings uncover previously undocumented morphological variation related to anuran ecological and locomotor diversification and link that variation to differences in jumping ability among species.
Genome size varies widely among organisms and is known to affect vertebrate development, morphology, and physiology. In amphibians, genome size is hypothesized to contribute to loss of late-forming ...structures, although this hypothesis has mainly been discussed in salamanders. Here we estimated genome size for 22 anuran species and combined this novel data set with existing genome size data for an additional 234 anuran species to determine whether larger genome size is associated with loss of a late-forming anuran sensory structure, the tympanic middle ear. We established that genome size is negatively correlated with development rate across 90 anuran species and found that genome size evolution is correlated with evolutionary loss of the middle ear bone (columella) among 241 species (224 eared and 17 earless). We further tested whether the development of the tympanic middle ear could be constrained by large cell sizes and small body sizes during key stages of tympanic middle ear development (metamorphosis). Together, our evidence suggests that larger genomes, slower development rate, and smaller body sizes at metamorphosis may contribute to the loss of the anuran tympanic middle ear. We conclude that increases in anuran genome size, although less drastic than those in salamanders, may affect development of late-forming traits.
Introduction: Shared selection pressures often explain convergent trait loss, yet anurans (frogs and toads) have lost their middle ears at least 38 times with no obvious shared selection pressures ...unifying “earless” taxa. Anuran tympanic middle ear loss is especially perplexing because acoustic communication is dominant within Anura and tympanic middle ears enhance airborne hearing in most tetrapods. Methods: Here, we use phylogenetic comparative methods to examine whether particular geographic ranges, microhabitats, activity patterns, or aspects of acoustic communication are associated with anuran tympanic middle ear loss. Results: Although we find some differences between the geographic ranges of eared and earless species on average, there is plenty of overlap between the geographic distributions of eared and earless species. Additionally, we find a higher prevalence of diurnality in earless species, but not all earless species are diurnal. We find no universal adaptive explanation for the many instances of anuran tympanic middle ear loss. Conclusion: The puzzling lack of universally shared selection pressures among earless species motivates discussion of alternative hypotheses, including genetic or developmental constraints, and the possibility that tympanic middle ear loss is maladaptive.
ABSTRACT When you take the time to observe another organism, there is a sort of gravity that can take hold, a mixture of curiosity and connection that expands and strengthens the more you interact ...with that organism. Yet, in research, a connection with one's study organism can, at times, feel countercultural. Study organisms are sometimes viewed more as tools to conveniently study biological questions. Here, we explicitly highlight the importance of organism-centered research not only in scientific discovery, but also in conservation and in the communication and perception of science.
Scheele
(Reports, 29 March 2019, p. 1459) bring needed attention to the effects of amphibian infectious disease. However, the data and methods implicating the disease chytridiomycosis in 501 ...amphibian species declines are deficient. Which species are affected, and how many, remains a critical unanswered question. Amphibians are imperiled; protective actions require public support and robust science.
Synopsis Terrestrial environments pose many challenges to organisms, but perhaps one of the greatest is the need to breathe while maintaining water balance. Breathing air requires thin, moist ...respiratory surfaces, and thus the conditions necessary for gas exchange are also responsible for high rates of water loss that lead to desiccation. Across the diversity of terrestrial life, water loss acts as a universal cost of gas exchange and thus imposes limits on respiration. Amphibians are known for being vulnerable to rapid desiccation, in part because they rely on thin, permeable skin for cutaneous respiration. Yet, we have a limited understanding of the relationship between water loss and gas exchange within and among amphibian species. In this study, we evaluated the hydric costs of respiration in amphibians using the transpiration ratio, which is defined as the ratio of water loss (mol H2O d−1) to gas uptake (mol O2 d−1). A high ratio suggests greater hydric costs relative to the amount of gas uptake. We compared the transpiration ratio of amphibians with that of other terrestrial organisms to determine whether amphibians had greater hydric costs of gas uptake relative to plants, insects, birds, and mammals. We also evaluated the effects of temperature, humidity, and body mass on the transpiration ratio both within and among amphibian species. We found that hydric costs of respiration in amphibians were two to four orders of magnitude higher than the hydric costs of plants, insects, birds, and mammals. We also discovered that larger amphibians had lower hydric costs than smaller amphibians, at both the species- and individual-level. Amphibians also reduced the hydric costs of respiration at warm temperatures, potentially reflecting adaptive strategies to avoid dehydration while also meeting the demands of higher metabolic rates. Our results suggest that cutaneous respiration is an inefficient mode of respiration that produces the highest hydric costs of respiration yet to be measured in terrestrial plants and animals. Yet, amphibians largely avoid these costs by selecting aquatic or moist environments, which may facilitate more independent evolution of water loss and gas exchange.
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