Phenotypic Variation through Ontogeny: Ceratophryid Frogs as a Model

Abstract

The South American frogs of the family Ceratophryidae (three genera, twelve extant species) display unusual larval diversity and developmental variation despite rather similar adults. Many adult features of ceratophryids are associated with terrestrial/fossorial habits and resistance to desiccation; however, adults of the genus Lepidobatrachus are aquatic. Morphological novelties have evolved in the ceratophryid feeding mechanism that makes them capable of feeding on exceptional large prey (i.e. megalophagy). Lepidobatrachus is unusual in having less ecomorphological differences between its larvae and adults than virtually all other anurans. Some unique features are differentiated in the tadpole and then exaggerated in the adult (e.g., a posterior displaced jaw articulation) in a manner unseen in other anurans. Both the larvae and the frog are similarly able to capture large prey underwater. The article reviews how shifts in developmental patterns have led to a novel way of life for both larval and adult Lepidobatrachus spp. Key Concepts Derived features of ceratophryid larvae carry over metamorphosis to the adults and are central to the overall morphological evolution of Ceratophryidae. Ceratophryidae shows how evolution can act upon development to produce organisms with novel structures and ecology. Megalophagy is associated with a wealth of other specialisations that are products of shifts in development. The origin of evolutionary novelties in Lepidobatrachus 's ontogeny has produced a dramatic and unique larval ecomorphology. Lepidobatrachus has broken metamorphic constraints to achieve common and shared larval and adult adaptations for megalophagy and feeding underwater.

Evolutionary and developmental considerations of the diet and gut morphology in ceratophryid tadpoles (Anura)

“…After 2 weeks as larvae, newly metamorphosed Lepidobatrachus reaches snout-vent length between 40 and 50 mm [12,13]. As previous authors have suggested, Lepidobatrachus has a life style in which larval and adult stages share a unique ecomorphology [9,10]. Lepidobatrachus larvae have a short alimentary tract with a dilated cranial segment with a distinct glandular surface that is both structurally and functionally like the adult stomach.…”

“…Tadpoles of ceratophryid genera are remarkably distinct, but they share accelerated developmental rates compared to tadpoles that are omnivorous and other taxa with obligated carnivorous tadpoles [6][7][8][9]. Carnivory has diversified in a manner unseen in other anurans since the Lepidobatrachus tadpole (with a massive gape) has become more like an adult [10].…”

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

“…Possibly environmental variations (especially those that can change significantly between field and lab conditions, such as feeding) may induce variation in presence and size of the appendix, and perhaps this exemplifies another case of environmental polyphenism such as that of scaphiopodids. A role in gas exchange in poorly oxygenated ponds was suggested for this structure (Fabrezi et al, ).…”

Genomic and Spectral Visual Adaptation in Southern Leopard Frogs during the Ontogenetic Transition from Aquatic to Terrestrial Light Environments

“…This strategy would be particularly relevant for frogs, which often have larval (tadpole) and adult phases that occupy very different ecological niches. Although previous studies have shown that morphological diversity of tadpoles and adult frogs is decoupled (Roelants, et al 2011; Sherratt, et al 2017; Wollenberg Valero, et al 2017; Fabrezi, et al 2019), studies testing for differences in gene expression are more limited (Wollenberg Valero, et al 2017). We found that a large proportion of the eye transcriptome (42%) was significantly differentially expressed between tadpole and juvenile southern leopard frogs, suggesting substantial, and potentially adaptive, decoupling at the level of gene expression.…”

“…Although both tadpole and adult ecologies vary extensively across the frog tree of life, most species have aquatic and herbivorous tadpoles, while adults are generally more terrestrial and carnivorous (McDiarmid and Altig 1999). A number of studies have shown that morphological diversity of tadpoles and adult frogs is decoupled (Roelants, et al 2011; Sherratt, et al 2017; Wollenberg Valero, et al 2017; Fabrezi, et al 2019) and that genetic correlations between tadpole and adult traits are low in many, but not all, cases (Blouin 1992; Phillips 1998; Watkins 2001; Goedert and Calsbeek 2019). However, several aspects of frog biology do tend to be coupled across life stages to varying degrees including behavior (Wilson and Krause 2012), size (Dehling and Sinsch 2019; Phung, et al 2020), and developmental plasticity (Trokovic, et al 2011).…”