Evolution of Rapid Development in Spadefoot Toads Is Unrelated to Arid Environments

Zeng, Cen; Gómez-Mestre, Iván; Wiens, John J.

doi:10.1371/journal.pone.0096637

Cited by 22 publications

(23 citation statements)

References 49 publications

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“…1b ) 13 , 16 , 17 . The short larval period with reduced plasticity of S. couchii represents a derived and canalized developmental state 16 , 22 . The divergence of reaction norms among spadefoot toad species is consistent with evolution by genetic accommodation of the timing of metamorphosis driven by selection in ponds with different hydroperiods 13 , 16 , 17 .…”

Section: Resultsmentioning

confidence: 99%

“…Thus, phenotypic differences among species in traits associated with the larval period mirror within-species differences caused by changes in developmental rate induced by pond drying and exogenous hormones. Further, based on phylogenetic character state reconstruction, plasticity in duration of the larval period is ancestral among extant spadefoot toad species, and rapid development in S. couchii is derived 16 , 22 . We therefore hypothesize that species differences in larval period and associated traits evolved through genetic accommodation via altered endocrine regulation.…”

Section: Introductionmentioning

confidence: 99%

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Genetic accommodation via modified endocrine signalling explains phenotypic divergence among spadefoot toad species

et al. 2017

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Phenotypic differences among species may evolve through genetic accommodation, but mechanisms accounting for this process are poorly understood. Here we compare hormonal variation underlying differences in the timing of metamorphosis among three spadefoot toads with different larval periods and responsiveness to pond drying. We find that, in response to pond drying, Pelobates cultripes and Spea multiplicata accelerate metamorphosis, increase standard metabolic rate (SMR), and elevate whole-body content of thyroid hormone (the primary morphogen controlling metamorphosis) and corticosterone (a stress hormone acting synergistically with thyroid hormone to accelerate metamorphosis). In contrast, Scaphiopus couchii has the shortest larval period, highest whole-body thyroid hormone and corticosterone content, and highest SMR, and these trait values are least affected by pond drying among the three species. Our findings support that the atypically rapid and canalized development of S. couchii evolved by genetic accommodation of endocrine pathways controlling metamorphosis, showing how phenotypic plasticity within species may evolve into trait variation among species.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Genetic accommodation via modified endocrine signalling explains phenotypic divergence among spadefoot toad species

et al. 2017

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“…Alternate interpretations challenge the hypothesis of an unequivocal relationship between arid environments and a short development to metamorphosis. In pelobatoid species, Buchholz and Hayes () and Zeng, Gomez‐Mestre, and Wiens () found that short larval periods and early hatching times are not significantly related to breeding in dry climates, but to small genome sizes and phylogeny. However, the authors specified that a strong relation might exist at the level of populations, or with respect to the presence of larvae in ephemeral versus permanent ponds.…”

Section: Discussionmentioning

confidence: 99%

Embryonic ontogeny of three species of Horned Frogs, with a review of early development in Ceratophryidae

Grosso

Baldo

Costa

et al. 2019

Journal of Morphology

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Horned Frogs of the family Ceratophryidae are conspicuous anurans represented by three endemic South American genera. Most ceratophryids inhabit semiarid environments, but three species of Ceratophrys occupy tropical or temperate humid areas. Several morphological and behavioral characters of larvae and adults are conserved across the family. Based on examination of specimens and accounts in the literature, the embryonic development of C. ornata, C. cranwelli, and the monotypic genus Chacophrys are described and compared with that of species of Lepidobatrachus. Ceratophryid embryos share a suite of morphological features and heterochronic shifts during development. Most features, such as gill structure, ciliation, early hatching, and precocious differentiation of the gut and hind limbs, are shared by all the species regardless the differences in the habitats that occupy. This is consistent with previous observations of some adult characters, and likely supports the hypothesis of an early diversification of ceratophryids in semiarid environments. Other embryonic features, such as the morphology and ontogeny of the oral disc and digestive tract, are correlated with larval feeding habits and vary within the family. The evolutionary and ecological significance of some conserved characters (e.g., gastrulation pattern, Type‐A adhesive glands) and other taxon‐specific features (e.g., nasal appendix) remain to be explored in the group.

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“…Conventionally, adaptation to this environment has been considered to rely on burrowing and rapid larval development. A recent study on extant scaphiopodids has shown that rapid larval development does not relate to climate, but to genome size and phylogeny 26 . Our study further casts doubt on the relationships between burrowing and aridity 5 6 .…”

Section: Discussionmentioning

confidence: 99%

A burrowing frog from the late Paleocene of Mongolia uncovers a deep history of spadefoot toads (Pelobatoidea) in East Asia

Chen

Bever

et al. 2016

Sci Rep

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Fossils are indispensible in understanding the evolutionary origins of the modern fauna. Crown-group spadefoot toads (Anura: Pelobatoidea) are the best-known fossorial frog clade to inhabit arid environments, with species utilizing a characteristic bony spade on their foot for burrowing. Endemic to the Northern Hemisphere, they are distributed across the Holarctic except East Asia. Here we report a rare fossil of a crown-group spadefoot toad from the late Paleocene of Mongolia. The phylogenetic analysis using both morphological and molecular information recovered this Asian fossil inside the modern North American pelobatoid clade Scaphiopodidae. The presence of a spade and the phylogenetic position of the new fossil frog strongly support its burrowing behavior. The late Paleocene age and other information suggestive of a mild climate cast doubt on the conventional assertion that burrowing evolved as an adaptation to aridity in spadefoot toads. Temporally and geographically, the new fossil provides the earliest record of Scaphiopodidae worldwide, and the only member of the group in Asia. Quantitative biogeographic analysis suggests that Scaphiopodidae, despite originating in North America, dispersed into East Asia via Beringia in the Early Cenozoic. The absence of spadefoot toads in East Asia today is a result of extinction.

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Evolution of Rapid Development in Spadefoot Toads Is Unrelated to Arid Environments

Cited by 22 publications

References 49 publications

Genetic accommodation via modified endocrine signalling explains phenotypic divergence among spadefoot toad species

Genetic accommodation via modified endocrine signalling explains phenotypic divergence among spadefoot toad species

Embryonic ontogeny of three species of Horned Frogs, with a review of early development in Ceratophryidae

A burrowing frog from the late Paleocene of Mongolia uncovers a deep history of spadefoot toads (Pelobatoidea) in East Asia

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