Underestimated anuran radiations in the high Andes: five new species and a new genus of Holoadeninae, and their phylogenetic relationships (Anura: Craugastoridae)

Abstract

Despite recent efforts to accelerate exploration and species description, the diversity of high Andean frogs remains highly underestimated. We report high levels of species diversity in direct-developing frogs or terraranas inhabiting the wet puna and adjacent cloud forests of the Amazonian versant of the Andes in Bolivia and Peru. Descriptive evidence of external morphology, distribution patterns and molecular phylogenetic analyses support the existence of nine unnamed species in two clades, which represents a 30% increase in species diversity for those clades. The relationships of these species and their relatives in Holoadeninae are tested using nuclear and mitochondrial genes for 159 terminals representing the 11 genera in this subfamily and 25 species of previously unknown relationships. Our results corroborate species monophyly in all but three cases and support the monophyly of all Holoadeninae genera, albeit the position of some differs between analyses. We propose a new genus (Microkayla gen. nov.) for the clade containing all Bolivian species formerly in Psychrophrynella plus five species from southern Peru. The new genus is monophyletic and supported by anatomical synapomorphies. Psychrophrynella is re-diagnosed and redefined to include three species from the Andes of southern Peru. We discuss the taxonomic instability associated with Noblella and Psychrophrynella due to the fact that the type species of both genera share a number of traits that support a close relationship. We also name and describe three new species of Bryophryne and two of Microkayla from Peru, provide baseline data for the future description of four Bolivian species of Microkayla, and describe the unknown mating calls of two species. Our results support that the grasslands of the Amazonian versant of the Andes harbour a large diversity of species with small altitudinal and horizontal distributions that replace each other along a latitudinal axis. These species belong to different lineages whose closest relatives are forest species, often from distant parts of the continent. These patterns suggest that high Andean environments were colonized several times independently by species with forest ancestors and which radiated into a multitude of species with remarkably similar ecomorphologies. The extent of these radiations remains obscured by a still rudimentary knowledge of species diversity due to insufficient fieldwork and taxonomic research.

A new species of Bryophryne (Anura: Strabomantidae) from the Cordillera de Vilcabamba, southeastern Peruvian Andes

“…Subsequently, the monophyletic status of the genus was corroborated by Chaparro (2015), De la Riva (2017), Heinicke (2017), and Padial (2014). Molecular evidence and distribution patterns have been strongly decisive in designation of new species and regrouping lineages (Hedges 2008, Padial 2012, Chaparro 2015, De la Riva et al 2017. Based on this evidence, the existence of three sympatric species of Bryophryne by mountain pass has been proposed (Lehr & Catenazzi 2008.…”

“…Hedges (2008), based on molecular data, proposed the monophyly of the genus and allocated it to the subfamily Holoadeninae; was designated as the type species. Subsequently, the monophyletic status of the genus was corroborated by Chaparro (2015), De la Riva (2017), Heinicke (2017), and Padial (2014). Molecular evidence and distribution patterns have been strongly decisive in designation of new species and regrouping lineages (Hedges 2008, Padial 2012, Chaparro 2015, De la Riva et al 2017.…”

“…Recent expeditions and published manuscripts show clear evidence of high beta diversity in the eastern slopes of the Peruvian and Bolivian Andes (De la Riva 2017, Rodriguez and. Most species of Bryophryne have been discovered in the last decade (Chaparro 2007, 2015, Lehr and Catenazzi 2008, 2010, De la Riva 2017, increasing the in the Archeological Complex of Choquequirao, Departamento Cusco has uncovered previously unknown species of Holoadeninae. Here we describe one of these new frogs, the third species of Bryophryne possessing a tympanic membrane and annulus and known to produce an advertisement call.…”

Peer Review #2 of "Evolutionary radiation of earless frogs in the Andes: molecular phylogenetics and habitat shifts in high-elevation terrestrial breeding frogs (v0.1)"

“…The first molecular phylogeny of Phrynopus (Lehr et al 2005) included eight currently recognized species in addition to five other species that were subsequently transferred to different genera (e.g., Phrynopus iatamasi was transferred to the genus Psychrophrynella by Hedges et al 2008, and it was subsequently transferred to the genus Microkayla by De la Riva et al 2017). Hedges et al (2008) inferred that Phrynopus is a close relative of the clades composed of Lynchius and Oreobates, a result corroborated by Padial et al (2014).…”

“…Given that species living in high-elevation habitats such as the Andean grassland appear to have larger body and different body shape than species living at lower elevations , we hypothesized that body size and body shape are associated with the type of habitat use and elevation. These direct-developing frogs are amenable for testing this hypothesis because they have low vagility (resulting in local genetic structuring) and in most cases limited geographic and elevational ranges (Duellman & Lehr 2009, De la Riva et al 2017. A larger body size at higher elevations would agree with Bergmann's rule, which predicts that body size increases in cooler environments (Bergmann 1847, Mayr 1956; this pattern requires further testing because it is not universal among amphibians (Adams & Church 2007).…”