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Pristimantis Lacrimosus Group (Anura, Strabomantidae) from the Eastern Slopes of the Ecuadorian Andes

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Pristimantis Lacrimosus Group (Anura, Strabomantidae) from the Eastern Slopes of the Ecuadorian Andes Evolutionary Systematics. 5 2021, 151–175 | DOI 10.3897/evolsyst.5.62661 A new cryptic species of the Pristimantis lacrimosus group (Anura, Strabomantidae) from the eastern slopes of the Ecuadorian Andes Julio C. Carrión-Olmedo1, Santiago R. Ron1 1 Museo de Zoología, Escuela de Ciencias Biológicas, Pontificia Universidad Católica del Ecuador, Av. 12 de Octubre y Roca, Aptdo. 17-01-2184, Quito, Ecuador http://zoobank.org/62F72992-7781-495B-8899-E72AE637ABD0 Corresponding author: Santiago R. Ron ([email protected]) Academic editor: Alexander Haas ♦ Received 11 January 2021 ♦ Accepted 6 May 2021 ♦ Published 23 July 2021 Abstract With 566 species, the neotropical genus Pristimantis is the most speciose vertebrate genus. As a result of its striking diversity, tax- onomic reviews remain a challenge. Herein, we present an updated phylogeny of the Pristimantis lacrimosus group and describe a new species from Llanganates and Sangay National Parks. We also report, for the first time, the phylogenetic position ofPristimantis degener, P. eugeniae, P. katoptroides, and P. petersi. Based on our phylogeny, we add two species to the Pristimantis lacrimosus group. Through the integration of molecular and bioacoustic evidence, we describe a new species which was hidden under “Pris- timantis petersi”. Pristimantis petersioides sp. nov. is most closely related to Pristimantis petersi and an undescribed species from Peru. It can be distinguished from P. petersi by its advertisement call and large genetic differences (uncorrected p-genetic distances 7.9% to 8.4% for gene 16S). Moreover, the new species and P. petersi are not sister species. We suggest assigning the new species to the Endangered Red List category because it has a small distribution range with deforestation as result of agriculture and other anthropogenic influences. Key Words Amphibia, Bioacoustics, Conservation, Diversity, National Parks, Phylogeny, Taxonomy Introduction Peters, 1863) and age are not as diverse suggesting that terrestrial breeding and Andean uplift are not the only The genus Pristimantis Jiménez de la Espada, 1870 has factors explaining the high diversity of Pristimantis. bewildered scientists for its striking diversity. Compris- The number of described species of Pristimantis is in- ing 566 Neotropical species it is the most speciose verte- creasing rapidly as result of the use of DNA sequences brate genus (Hedges et al. 2008; Frost 2021). In Ecuador, allowing the discovery of a large number of cryptic spe- this genus encompasses more than one third of all anuran cies. DNA sequences helps to achieve better informed species, with 233 out of 640 species (Ron et al. 2019). taxonomic decisions and speed up species discovery The astounding species richness of Pristimantis has with more than 40 species of Pristimantis (e.g. Orte- been attributed to terrestrial breeding – direct embryonic ga et al. 2015; Guayasamin et al. 2017; Páez and Ron development without a tadpole stage (Padial et al. 2014) 2019) described in Ecuador in the last five years. In some – and the appearance of geographic barriers as result of clades, the number of undescribed species outnumbers the Andean uplift (Lynch and Duellman 1997; Mendo- described species (e.g., Ortega et al. 2015; Páez and Ron za et al. 2015). However, other sympatric Andean gen- 2019) suggesting that there could be hundreds of unde- era with similar reproductive mode (e.g., Strabomantis scribed species of Pristimantis. Copyright Julio C. Carrión-Olmedo, Santiago R. Ron. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 152 Julio C. Carrión-Olmedo & Santiago R. Ron: New species of Pristimantis from Andean Ecuador Taxonomy within this group have been problemat- Pristimantis petersi holotype (KU 143508) is from ic and unstable because most species descriptions have 16.5 km NNE of Santa Rosa, Napo Province, 1700 m. been based on morphological traits (Lynch and Duellman However, most specimens used in the species description 1997), which can be highly variable and homoplastic (e.g. by Lynch and Duellman (1980) were from other popula- Guayasamin et al. 2015; Páez and Ron 2019). Taxonomic tions including localities in the central Andes of Colombia problems in Pristimantis are still pervasive and are still (Huila and Putumayo Departments), and central Ecuador far from being fully resolved (e.g., Páez and Ron 2019; (Napo and Pastaza provinces). As currently defined, Pris- Reyes-Puig et al. 2019; Moravec et al. 2020). timantis petersi is considered to have a wide distribution One clade of Pristimantis containing undescribed from the central Andes of Colombia (Lynch and Duell- species is the Pristimantis lacrimosus species group man 1980; Mueses-Cisneros 2005; Stuart et al. 2008) to (Ron et al. 2020). Hedges et al. (2008) proposed it as the eastern slopes of the Ecuadorian Andes, from Sucum- monophyletic based on molecular data from only three bíos to Morona Santiago Provinces at altitudes ranging species. However, more recent phylogenies with better between 1400–2000 m a.s.l (Brito et al. 2017; Ron et al. species sampling showed that this group was paraphy- 2019). Lynch and Duellman (1980) mentioned that Pristi- letic (Padial et al. 2014; Rivera-Correa and Daza 2016). mantis petersi exhibits body size variation throughout its Rivera-Correa and Daza (2016) identified two non-sis- distribution range and, remarkably, realized that individ- ter clades within the Pristimantis lacrimosus species uals from the upper Pastaza trench were larger than indi- group, “clade A” endemic to Colombia and “clade B” viduals from the type locality, Ecuador, and suspected that composed by species from Central America, Ecuador, populations from Pastaza may represent another species. and Peru. González-Durán et al. (2017) proposed the The wide geographic distribution of Pristimantis pe- Pristimantis boulengeri group for “clade A” and hy- tersi suggest that it may be a species complex. Recent pothesized that “clade B” corresponds to the P. lacrimo- reviews of Andean Pristimantis suggest that most spe- sus species group. That assignment was questioned by cies have highly restricted distributions. For example, Rivera-Correa and Daza (2020) but was demonstrated in the subgenus Huicundomantis Páez & Ron, 2019 all as correct by Ron et al. (2020) who included in their species had distribution ranges below 5000 km2 and the phylogeny, for the first time, the type species for the seemingly large distribution of “P. phoxocephalus” and group, P. lacrimosus (Jiménez de la Espada, 1875). Ron “P. riveti” were an artifact of the combined distribution et al. (2020) also described three new species and re- of several cryptic species (Páez and Ron 2019). Simi- defined the group to include all descendant species of larly, “P. calcarulatus” was considered to be distributed the most recent common ancestor of P. eremitus (Lynch, in the Andes from central Ecuador to southern Colom- 1980) and P. lacrimosus for a total of 36 formally de- bia (Hutter and Guayasamin 2015). However, genetic scribed species. and morphological evidence demonstrated that “P. cal- Despite these advances, there still are species of the carulatus” was a complex of three different species, Pristimantis lacrimosus group which have never been each with a small distribution range. Similar results included in molecular phylogenies. One of them is have been found within “P. orestes”, “P. ornatissimus” Pristimantis petersi (Lynch & Duellman, 1980). Since (Guayasamin et al. 2017; Urgiles et al. 2019), and P. its description, this species suffered several taxonomic ventrimarmoratus (Moravec et al. 2020). It is unclear changes. Lynch (1991) changed its name to Eleuthero- if species of Andean Pristimantis with large distribu- dactylus petersorum to avoid homonymy with a Mexi- tions (> 10000 km2) actually exist. We are unaware of can species with the same epithet, which now is known any species of Pristimantis with such distribution with- as Eleutherodactylus nitidus (Peters 1870). Additionally, standing a taxonomic review based on genetic and phe- Lynch (1996) created the name Eleutherodactylus john- notypic characters. The available evidence suggests that wrighti, as an amend to the previous epithet petersorum. species with seemingly large distributions, like P. peter- Afterwards, Frost (2009) applied Article 59.4 of the In- si, may represent species complexes. ternational Code of Zoological Nomenclature making The existence of cryptic diversity within P. petersi is Eleutherodactylus johnwrighti and Eleutherodactylus pe- also suggested by reports of body size differences among tersorum invalid replacement names because the taxa in populations of P. petersi (Lynch and Duellman 1980; question are not congeneric and recovered the first epithet Brito et al. 2017). Recent fieldwork conducted by field used for this species. staff of the QCAZmuseum from Pontificia Universidad Pristimantis petersi has been usually assigned to the Católica del Ecuador resulted in collections of P. petersi P. lacrimosus species group. Lynch and Duellman (1980) near its type locality and in the discovery of populations placed it in the P. unistrigatus group, P. lacrimosus assem- of a species similar to P. petersi in Sangay National Park bly. Later, Lynch and Duellman (1997) placed it in the un- and Llanganates National Park. Through the integration
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