Growth and cranial development in the Andean frogs of the genus Telmatobius (Anura: Telmatobiidae): Exploring the relation of heterochrony and skeletal diversity

Abstract

Andean frogs of the genus Telmatobius occur at high elevations, they have an aquatic mode of life and large tadpoles. There are more than 60 species that closely resemble one another and have low values of genetic divergence. However, the skeleton, particularly the cranium, is interspecifically variable with respect to the different levels of development of some elements. Heterochrony is considered to have played a prominent role in generating phenotypic variation, especially among closely related species. Herein, the developmental origins of the adult cranial configuration of two species of Telmatobius are explored. The interactions among larval and postmetamorphic growth, sexual maturation, and ossification sequence in T. oxycephalus and T. rubigo are studied. Although there are no substantial changes in the sequences of ossification of the cranium, it is likely that differential timing of larval periods is related to adult cranial characters. The prolonged larval development of T. rubigo may result in peramorphic configurations of bones that ossify during pre-metamorphosis. This long developmental time would also explain why the gonads of T. rubigo are highly differentiated by the end of metamorphosis. In this species, sexual maturation may be attained precociously in relation to metamorphosis, thereby reducing postmetamorphic developmental time of late-onset bones, which have paedomorphic configurations (e.g., vomer, neopalatine, and columella). An inverse pattern characterizes T. oxycephalus, suggesting that the duration of larval life is related to skeletal configuration in Telmatobius.

Variation in the growth and development of the hind limbs in frogs of the genus Telmatobius (Anura: Telmatobiidae)

“…One of the most striking differences between these two species is that the tadpoles of Telmatobius rubigo are significantly larger than those of T. oxycephalus at any given stage (Barrionuevo, 2018). , 1981), and especially the ossification of the bones (Kemp & Hoyt, 1969;Terry, 1918).…”

“…The gonads are more highly differentiated than in T. oxycephalus and (ii) at the onset of sexual maturity. Individual T. rubigo have reached only 30% of their maximum postmetamorphic size versus the 40% in T. oxycephalus (Barrionuevo, 2018). The shorter juvenile life signals a shorter period with a favorable rate of development of hind limbs over the body Buchholz, 2006;Márquez-García et al, 2009;Newman, 1989;Richter-Boix, Llorente, & Montori, 2006).…”

“…Thus, it is appropriate to speculate on the proximate factors that influence the most obvious phenotypic differences between these two species. Recently, it has been proposed that differences in the timing of larval development influence postmetamorphic morphology of the cranium and middle ear in these species (Barrionuevo, 2018). Variation in the morphology of the hind F I G U R E 1 Box plots of length of the four hind limb segments (femur, tibia, tarsus, and foot) relative to SVL in Telmatobius oxycephalus and T. rubigo.…”

“…Species of Telmatobius have large larvae, and interspecifically, there are remarkable differences in the maximum larval size at comparable stages (Aguilar & Lehr, 2009; Barrionuevo, 2018; Barrionuevo & Baldo, 2009; Fernández, 1927). Telmatobius oxycephalus and T. rubigo are good examples of disparity in larval size at comparable stages (Gosner, 1960), with the larvae of T. rubigo being significantly larger than those of T. oxycephalus .…”

“…Telmatobius oxycephalus and T. rubigo are good examples of disparity in larval size at comparable stages (Gosner, 1960), with the larvae of T. rubigo being significantly larger than those of T. oxycephalus . After Stage 40 in T. rubigo , the maximum total larval size is 113 mm and the larval body size 38 mm, whereas in T. oxycephalus , these lengths are 76 mm and 27 mm, respectively (Barrionuevo, 2018). The ranges of these species are adjacent to one another and both inhabit montane streams, but the species are separated elevationally; T. oxycephalus is found at intermediate elevations from 1,500–2,800 m., whereas T. rubigo occurs at higher elevations between 3,500 and 4,100 m.…”