1 3 Recent evolutionary history of Lost World endemics: Population 4 genetics, species delimitation, and phylogeography of sky-island 5 treefrogs 6 7 8 P.E. Salerno a,⇑ Q1 , J.C. Señaris b , F.J.M. Rojas-Runjaic c , D.C. Cannatella a 9 a Department of Integrative Biology and Texas Natural History Collections, University of Texas at Austin, 1, University Station, C0990, Austin, TX 78712, USA 10 b Centro de Ecología, Instituto Venezolano de Investigaciones Científicas, Apartado 20632, Caracas 1020-A, Venezuela 11 c Museo de Historia Natural La Salle, final Av. Maripérez con Av. Boyacá (Cota Mil), Apartado Postal 1930, Caracas 1010-A, Venezuela 12 13 14 16 article info 17 Article history: 18 Received 5 June 2014 19 Revised 22 October 2014 20 Accepted 25 October 2014 21 Available online xxxx 22 Keywords: 23 Tepui 24 Tepuihyla 25 Coalescent 26 Species delimitation 27 Haplotype diversity 28 29 abstract 30 The tepuis of South America are massive flattop mountains with cliffs up to 1000 m and summit up to 31 3100 m. Tepuis hold enormous endemicity levels, but little is known about the origins of the endemic 32 flora and fauna. Recently diverged lineages offer the possibility of understanding the origins of summit 33 endemicity by examining population dynamics and dispersal. We examine species delimitation, clade 34 relationships, and demographic patterns of three recently diverged lineages of Tepuihyla, an endemic 35 treefrog clade. These three lineages represent two currently recognized species, T. edelcae and T. rodri- 36 guezi. Given the low divergences in both nuclear and mitochondrial genes among lineages, we find unex- 37 pectedly high numbers of unique nuclear haplotypes and moderate levels of lineage sorting. We also find 38 support from multiple analyses for a cryptic, undescribed summit species within T. edelcae. We suggest 39 that the genetic and distribution patterns of the four most recently diverged Tepuihyla lineages support a 40 concurrent speciation event during the Pliocene, and suggest a biogeographic hypothesis in which a 41 widespread climatic change made mid- and low-elevation habitat unsuitable for the common ancestor 42 within the timeframe of their divergence. 43 Ó 2014 Published by Elsevier Inc. 44 45 46 47 1. Introduction 48 Montane regions harbor many of the global hotspots of diver- 49 sity, yet the extent of diversity is not fully appreciated because 50 many regions are inaccessible. The flattop mountains (tepuis) of 51 northern South America form an endemicity hotspot that remains 52 largely unexplored. Researchers traditionally believed that the 53 summit biota of the tepuis—the ‘‘Lost World’’ that inspired Conan 54 Doyle’s book of the same name—has been isolated atop summits 55 since their formation. However, molecular analyses indicate that 56 the Lost World is not as isolated and ‘‘prehistoric’’ as popularly 57 thought (Givnish et al., 1997; Rull, 2004; Kok et al., 2012; 58 Salerno et al., 2012; Bonaccorso and Guayasamin, 2013), though 59 much remains to be done to elucidate the evolutionary history of 60 this fascinating sky-island ecosystem and the causes of its 61 enormous endemicity. 62 The tepuis are remnants of the Precambrian Guiana Shield pla- 63 teau, which encompasses a large area of South America east of the 64 Andes and north of the Amazon River basin. These sandstone table 65 mountains were formed approximately 60–90 mya after many 66 cycles of erosion of the Guiana Shield plateau, starting around 67 300 mya. These remnants form hundreds of sky-islands that reach 68 up to 3000 m, with walls up to 1000 m high. Hundreds of kilome- 69 ters of drastically different lowlands separate most summits 70 (Briceño et al., 1990; Briceño and Schubert, 1990; Gibbs and 71 Barron, 1993). Thus, tepuis form a discontinuous ecosystem of 72 sky-islands called Pantepui (Mayr and Phelps, 1955; Huber, 73 1988), similar to yet arguably much more extreme in topography 74 than other well-known sky-island systems such as the Rocky 75 Mountains and the Western Ghats (DeChaine and Martin, 2005; 76 Smith and Farrell, 2005; Robin et al., 2010). 77 The Pantepui holds enormous endemicity of many taxa, partic- 78 ularly frogs (77%; McDiarmid and Donnelly, 2005) and plants 79 (60%; Huber, 1988; Berry and Riina, 2005). Traditionally, the high 80 endemism has been explained by the Lost World Hypothesis 81 (Chapman, 1931; Maguire, 1970; Rull, 2004; McDiarmid and 82 Donnelly, 2005). However, accumulating evidence strongly http://dx.doi.org/10.1016/j.ympev.2014.10.020 1055-7903/Ó 2014 Published by Elsevier Inc. ⇑ Corresponding author. E-mail addresses: patriciasalerno@gmail.com (P.E. Salerno), jsenaris@ivic.gob.ve (J.C. Señaris), rojas_runjaic@yahoo.com (F.J.M. Rojas-Runjaic), catfish@austin. utexas.edu (D.C. Cannatella). Molecular Phylogenetics and Evolution xxx (2014) xxx–xxx Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev YMPEV 5060 No. of Pages 10, Model 5G 7 November 2014 Please cite this article in press as: Salerno, P.E., et al. Recent evolutionary history of Lost World endemics: Population genetics, species delimitation, and phylogeography of sky-island treefrogs. Mol. Phylogenet. Evol. (2014), http://dx.doi.org/10.1016/j.ympev.2014.10.020