Holoadeninae, Hedges, Duellman & Heinicke, 2008

Padial, José M., Grant, Taran & Frost, Darrel R., 2014, Molecular systematics of terraranas (Anura: Brachycephaloidea) with an assessment of the effects of alignment and optimality criteria, Zootaxa 3825 (1), pp. 1-132 : 53

Holoadeninae

This taxon includes all genera placed in Holoadeninae by Hedges et al. (2008a) ( Barycholos , Bryophryne , Euparkerella , Holoaden , Noblella , and Psychrophrynella ), plus a clade ( Lynchius , Oreobates , and Phrynopus ) placed in Strabomantinae by Hedges et al. (2008a) and Pristimantinae by Pyron & Wiens (2011), with Hypodactylus as sister of all other genera. By including Hypodactylus , Lynchius , Oreobates , and Phrynopus in this subfamily, we rectify the non-monophyly of Pristimantinae of Pyron & Wiens (2011) and alter the incertae sedis status of Hypodactylus . DNA sequences for Niceforonia are unavailable. However, Hedges et al. (2008a) assigned Niceforonia to Strabomantinae on the basis of a synapomorphic character-state (knobbed rather than T-shaped terminal phalanges) that unites it to the Lynchius , Oreobates , and Phrynopus clade, so we also refer Niceforonia to Holoadeninae .

Lehr et al. 's (2005) maximum likelihood analyses of molecular data first suggested the existence of this inclusive group by recovering a clade containing Hypodactylus , Phrynopus , Psychrophrynella , and Noblella . More recently, Canedo & Haddad (2012) found Euparkerella brasiliensis to be the sister of Holoaden and “ Eleutherodactylus bilineatus ” to be the sister of the clade formed by Noblella and Barycholos (and, therefore, part of our Holoadeninae ). Until recently, “ Eleutherodactylus bilineatus ” was considered a taxon of uncertain affinities ( Lynch and Myers 1983; Lynch & Duellman, 1997) and was tentatively placed in Ischnocnema by Heinicke et al. (2007). Unfortunately, sequences of “ E. bilineatus ” and Euparkerella were not available when we undertook the analyses for the present study.

Although no morphological synapomorphies are known to delimit this morphologically diverse group, several of the relationships recovered by molecular evidence within this clade were recognized in early morphological studies. In content, Holoadeninae roughly approximates Phrynopus of Lynch (1975), a genus that, besides Phrynopus sensu stricto, included species now placed in the genera Bryophryne , Hypodactylus , Lynchius , Niceforonia , Noblella , Oreobates , Psychrophrynella , Phrynopus , and Pristimantis . Lynch (1971) considered Euparkerella to be related to Holoaden because they both lack the alary process of the hyoid plate, a relationship later recovered by Ardila-Robayo (1979) and more recently by Canedo & Haddad (2012). Lynch (1973) also suggested that Leptodactylus mantipus Boulenger (now Hypodactylus mantipus ) should be included in Barycholos because of the shared presence of a posteriorly bifurcate sternal style. Nevertheless, Heyer (1975) rejected that view based on his morphological observations that suggested that another Hypodactylus ( H. nigrovittatus ) and Barycholos pulcher were sister taxa. Hypodactylus nigrovittatus has yet to be included in a molecular phylogenetic study, and a relationship with B. pulcher is still likely. Lynch (1976b) named two species of Euparkerella , for which Heyer (1980) later erected the genus Phyllonastes , subsequently synonymized by De la Riva et al. (2008) with Noblella . Lynch (1986b) considered Phrynopus bagrecito (now in Psychrophrynella ) to be closely related to Phyllonastes heyeri (now in Noblella ).

A remarkable characteristic of this clade is the recurrent connection of taxa found in the Atlantic Forest in southeastern Brazil and in the Andes, as suggested by the relationships within Oreobates (Andes, Amazonia, and southeastern Brazil) and the clade composed of Holoaden ( Ecuador and southeastern Brazil), Euparkerella (southeastern Brazil), Bryophryne (Andes) , " Eleutherodactylus " bilineatus (southeastern Brazil), Noblella (Andes) , and Barycholos (southeastern Brazil).