Early ontogeny and sequence heterochronies in Leiuperinae frogs (Anura: Leptodactylidae)

Abstract

The study of early development in Neotropical Leiuperinae frogs (Anura, Leptodactylidae) has been addressed by several works in recent times. However, a comparative developmental approach under a phylogenetic context was not available. Herein we analyzed the morphological and ontogenetic diversity of embryos belonging to 22 species of the three largest genera in Leiuperinae. We find that in most cases, variations fit with the phylogeny at the inter- and intrageneric levels. Embryo kyphosis and whitish color are synapomorphies for the clade grouping Physalaemus and Engystomops . The presence of a third lower tooth row on the oral disc is plesiomorphic for Leiuperinae, only changing in derived clades. The configurations and developmental trajectories of the lower lip are exceptionally diverse. The developmental sequences optimized on the phylogenetic tree recover an early differentiated first lower tooth row a synapomorphy of Pseudopaludicola and Physalaemus , and an early differentiated second row as synapomorphy of Pleurodema . On the other hand, few features are highly conserved in the subfamily, such as the adhesive glands universally present in a type-C configuration. Our results also suggest that the morphology and ontogeny of embryos is in some cases associated to the environment where they develop. A large body size, poorly developed transient respiratory structures, large yolk provision and delayed development of the digestive tract occur convergently in embryos inhabiting cold, oxygenated environments. Embryos that develop in warmer water bodies in xeric environments show more complex and persistent transient respiratory structures and an early onset of hind limbs development. Our survey highlights that morphology and early development of anurans can be a valuable source of information for phylogenetic studies, and provide fundamental bases to explore and discuss how evolutionary changes can be shaped by environmental conditions.

Temperature and development drive variation in oral morphology among tailed frog (Ascaphusspp.) populations

“…Indeed, the relationship between size and developmental stage only represents one aspect of development. Changes in the sequence, rate, or timing of developmental events can lead to phenotypic variation (Chipman et al, 2000;Chipman, 2002), including in oral morphology (Vera Candioti et al, 2011;Grosso et al, 2019). Differences in developmental trajectories due to these proximate mechanisms may be contributing to the variation observed in this study or explain the opposing relationships between labial teeth number and our developmental proxy.…”

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

“…The early onset of gut coiling and active feeding, and the regression of the anal tube predisplaced to prometamorphic larval stages (Fabrezi & Quinzio, 2008) also are consistent with this. As in ceratophryids, hind-limb differentiation and the onset of active feeding occur early in the developmental trajectories of scaphiopodids (Buchholz & Hayes, 2002;Hall et al, 1997) and leiuperines from dry areas (Figure 8; Grosso et al, 2019). Developmental acceleration is achieved by the synergy of increasing levels of corticosterone and thyroid hormones on target tissues such as the limbs and gut (e.g., Wen et al, 2017).…”

“…Some embryonic features of ceratophryid frogs described here have been discussed in the context of development in bodies of water in xeric environments, which tend to be unstable, warm, and poorly oxygenated. For example, long, branched gills and profuse, long‐lasting ciliation are convergent characters of some foam‐nest leiuperine embryos that inhabit brackish ponds of the South American Chaco and the Brazilian Caatinga (Grosso et al, ). Embryos of the Spadefoot toad, Spea intermontana , also remain highly ciliated after gill regression (Hall, Larsen Jr, & Fitzner, ).…”

“…In addition, we collected and examined five young tadpoles of Lepidobatrachus asper Budgett to compare some developmental events with those of the complete series of the remaining species. We also included developmental series of Boana riojana (Koslowsky) (Hylidae), Odontophrynus americanus (Dúmeril and Bibron) (Odontophrynidae), and material of three leiuperine species (Leptodactylidae) from an earlier contribution (Grosso et al, ) to be used as outgroups in the analyses. Data for all specimens examined (including permits for collecting, maintaining and reproducing animals) appear in Supporting Information; Appendix S1.…”

Development of a non-amphibious amphibian - an interview with a coquí

“…Gastrotheca riobambae and Eleutherodactylus coqui have been most frequently involved (Elinson and del Pino 2012), and Lepidobatrachus laevis (Bloom et al 2013;Amin et al 2015) has attracted attention recently. There are many others, whose interesting life histories promise to provide unique perspectives (Araújo et al 2016;Fabrezi et al 2010Fabrezi et al , 2016Goldberg and Vera Candioti 2015;Goldberg et al 2012;Grosso et al 2019).…”