Phylogenetic systematics of egg-brooding frogs (Anura: Hemiphractidae) and the evolution of direct development

Abstract

Egg-brooding frogs (Hemiphractidae) are a group of 105 currently recognized Neotropical species, with a remarkable diversity of developmental modes, from direct development to free-living and exotrophic tadpoles. Females carry their eggs on the back and embryos have unique bell-shaped gills. We inferred the evolutionary relationships of these frogs and used the resulting phylogeny to review their taxonomy and test hypotheses on the evolution of developmental modes and bell-shaped gills. Our inferences relied on a total evidence parsimony analysis of DNA sequences of up to 20 mitochondrial and nuclear genes (analyzed under tree-alignment), and 51 phenotypic characters sampled for 83% of currently valid hemiphractid species. Our analyses rendered a well-resolved phylogeny, with both Hemiphractidae (sister of Athesphatanura) and its six recognized genera being monophyletic. We also inferred novel intergeneric relationships [((Cryptobatrachus, Flectonotus), (Stefania, (Fritziana, (Hemiphractus, Gastrotheca))))], the non-monophyly of all species groups previously proposed within Gastrotheca and Stefania, and the existence of several putative new species within Fritziana and Hemiphractus. Contrary to previous hypotheses, our results support the most recent common ancestor of hemiphractids as a direct-developer. Free-living aquatic tadpoles apparently evolved from direct-developing ancestors three to eight times. Embryos of the sister taxa Cryptobatrachus and Flectonotus share a pair of single gills derived from branchial arch I, while embryos of the clade including the other four genera have two pairs of gills derived from branchial arches I and II respectively. Furthermore, in Gastrotheca the fusion of the two pairs of gills is a putative synapomorphy. We propose a revised taxonomy concordant with our optimal topologies.

Evolution in the South American ‘Lost World’: insights from multilocus phylogeography of stefanias (Anura, Hemiphractidae, Stefania)

“…(), followed by Castroviejo‐Fisher et al . (), showed that, based on molecular data, these groups were not reciprocally monophyletic. Rivero () extensively discussed the possible origin, endemism, and distribution of the genus.…”

“…Castroviejo‐Fisher et al . () found the genus as sister to a clade containing Fritziana , Hemiphractus and Gastrotheca . The genus Stefania itself has never been the subject of rigorous molecular phylogenetic analyses, mainly because of a lack of comprehensive sampling.…”

“…Both groups were still recognized until recently (e.g. MacCulloch et al, 2006) when Kok et al (2012), followed by Castroviejo-Fisher et al (2015), showed that, based on molecular data, these groups were not reciprocally monophyletic. Rivero (1970) extensively discussed the possible origin, endemism, and distribution of the genus.…”

Pouch brooding marsupial frogs transfer nutrients to developing embryos

“…Marsupial frogs are of great interest to developmental and evolutionary biologists because of the potential reversal in reproductive modes from live-bearing to tadpole development [22]. Our findings show that ancestral features for gas exchange for developing embryos may be co-opted via convergent evolution for nutrient transfer [7], and suggest that greater exploration of the diverse reproductive modes among marsupial frogs could provide insight into the evolution of matrotrophy in vertebrates.…”

Fritziana ulei (Miranda-Ribeiro, 1926): geographic extension, with comments on the natural history of this species

“…The genus Fritziana Mello-Leitão, 1937 is endemic of the Atlantic Rainforest (Folly et al 2014) where it is occurs in the lowlands and on slopes of the coastal mountains to elevations of 2200 m in southeastern Brazil (Duellman 2015). It is composed by five species, F. goeldii (Boulenger, 1895), F. ohausi (Wandolleck, 1907, F. fissilis (Miranda-Ribeiro, 1920), F. tonimi Walker, Gasparini & Haddad, 2016, and F. ulei (Miranda-Ribeiro, 1926 (Castroviejo-Fisher et al 2015). Fritziana spp.…”