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The taxonomic and phylogenetic status of some poorly known Anolis from the Andes of with the description of a nomen nudum taxon

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The user has requested enhancement of the downloaded file. Zootaxa 4303 (2): 213–230 ISSN 1175-5326 (print edition) http://www.mapress.com/j/zt/ Article ZOOTAXA Copyright © 2017 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4303.2.2 http://zoobank.org/urn:lsid:zoobank.org:pub:6BB7825C-94F0-431E-A338-BFC9218076F4

The taxonomic and phylogenetic status of some poorly known Anolis species from the Andes of Colombia with the description of a nomen nudum taxon

FREDDY A. GRISALES-MARTÍNEZ1,5, JULIÁN A. VELASCO2, WILMAR BOLÍVAR3, ERNEST E. WILLIAMS4 & JUAN M. DAZA1,6 1Grupo Herpetológico de Antioquia, Instituto de Biología, Universidad de Antioquia, Calle 67 # 53–108, Bloque 7–121, A.A. 1226, Medellín, Colombia. 2Museo de Zoología “Alfonso L. Herrera”, Facultad de Ciencias, Universidad Nacional Autónoma de México, Mexico city, Mexico. 3Grupo de Ecología , Departamento de Biología, Universidad del Valle, Cali, Colombia 4Williams is included as posthumous author as this paper includes part of his unpublished manuscript. 5Servicios Ambientales y Geográficos S.A., Calle 11B # 40A-130, Piso 4, Medellín, Colombia. 6Corresponding author. E-mail: [email protected]

Abstract

We studied the phylogenetic status, morphological variation, dewlap color variation, and geographic distribution of four poorly known Anolis species nested in the Norops clade, particularly in the A. fuscoauratus group from the Andes of Co- lombia. In addition, we also describe a nomen nudum species based on morphological and molecular evidence. This nomen nudum taxa differ from other fuscoauratoids species in a combination of dewlap color, meristic traits, and molecular evi- dence. Our integrative analysis (molecular phylogenetics, morphology, and dewlap color) revealed the non-monophyletic status of these Andean taxa. We also confirmed the occurrence of A. fuscoauratus in the Magdalena valley in Colombia (a trans-Andean region). Our findings show that the evolution of Andean anoles is more complex than previously thought and more research is necessary to understand the diversity in this cryptic group.

Key words: Geographic distribution, molecular phylogenetics, morphology, Neotropical region,

Resumen

Estudiamos el estatus filogenético, la variación morfológica, la variación cromática del abanico gular y la distribución geográfica de varias especies Anolis poco conocidas del clado Norops, particularmente en el grupo A. fuscoauratus de los Andes de Colombia. Adicionalmente describimos una especie nomen nudum basada en evidencia morfológica y molecu- lar. Este taxón nomen nudum difiere de otras especies de fuscoauratoides en una combinación de coloración del abanico gular, caracteres merísticos y evidencia molecular. Nuestro análisis integrativo (filogenética molecular, morfología y col- oración del abaníco gular) reveló el estado no monofilético de estos taxones andinos. También, confirmamos la presencia de Anolis fuscoauratus en el valle del Magdalena en Colombia (región Trans-Andina). Nuestros hallazgos muestran que la evolución de los Anolis andinos es más compleja de lo pensado y que más investigación es necesaria para entender la diversidad en este grupo críptico.

Palabras clave: Distribución geográfica, filogenética molecular, morfología, región Neotropical, taxonomía de lagartos

Introduction

The Anolis genus is a highly diverse group of vertebrates, with more than 400 species currently recognized (Uetz et al. 2017). Many of these species occurs in mainland settings where in the recent years many species have been described as a result of extensive fieldwork in poorly surveyed areas (e.g., Colombia) and detailed examination of specimens in some regional herpetological collections (Velasco & Hurtado-Gómez 2014).

Accepted by L. Avila: 17 May 2017; published: 9 Aug. 2017 213 Furthermore, some species were named in the past by E. E. Williams and were never formally published (see Ayala 1986). Although almost all nomen nudum species were described in the last decades (A. ruizi Rueda & Williams 1986; A. danieli Williams 1988; A. medemi Ayala & Williams 1988; A. lamari Williams 1992; A. anchicayae and A. lyra Poe at al. 2009), or were synonymized (A. “jericoensis” Ayala 1986 with A. eulaemus Boulenger 1908; A. “malkini” Ayala 1986 with A. pentaprion Cope 1863; see Poe et al. 2009), others still remain to be formally described (Poe et al. 2009). The Anolis fuscoauratus species group was originally defined by Williams (1976) based on a combination of meristic traits. This group is distributed in Central America, northern South America and the entire Amazon basin and putatively is composed by 22 species (Williams 1976; Ayala & Williams 1988; Savage 2002; Nicholson 2002). Within this large group, a small group distributed in the Andes region and composed of three species: A. mariarum Barbour 1932, A. antonii Boulenger 1908, and A. tolimensis Werner 1916. Ayala (1986) mentioned a fourth name for a fuscoauratoid restricted to the western part of the Northern Andes in Colombia, particularly in the Urrao municipality. Although these Andean anoles are very similar in external morphology and body coloration, there are notable differences in dewlap color between species (Ayala & Williams 1988; Arosemena & Ibáñez 1993). In addition, the geographic distribution is not completely known for these taxa. In recent phylogenetic studies found that the Anolis fuscoauratus group is polyphyletic (Nicholson 2002; Poe 2004; Nicholson et al. 2012). In a recent phylogenetic approach including some species from the A. fuscoauratus group, it was found that A. tolimensis was not nested with A. antonii and A. mariarum (Poe et al. 2017). In this study, using molecular data we infer the phylogenetic position of four Andean taxa (A. antonii, A. mariarum, A. tolimensis, and the nomen nudum Anolis urraoi) within other closely related fuscoauratoids from the Amazon basin and Central America (Poe et al. 2017). We conduct a statistical morphometric analysis and also describe the color variation. For our comparative analyses, we include specimens from type localities for each species for all comparative analyses (phylogeny, morphology, and color).

Materials and methods

Taxon sampling. We examined specimens from the herpetological collections of Colegio San Jose de Medellín (CSJ), Museo de Herpetología Universidad de Antioquia (MHUA) and Colección de Docencia Universidad del Valle (CZPD) (Appendix 1). Here, we adopt the evolutionary species concept (Wiley 1978), which is operationalized based on substantial and consistent differences among populations. We adopt the criteria outlined by Wiens & Servedio (2000) consisting of recognizing populations as distinct evolutionary lineages based on the frequency of traits allowing polymorphism. This criterion is more realistic to delimitate species than others criteria based on fixed traits (Wiens & Servedio 2000). We mapped all the examined specimens in ArcMap 9.3 (ESRI 2008). We compared the new species with the three Andean fuscoauratoids currently recognized (A. antonii, A. mariarum, and A. tolimensis). Data of coloration in life were obtained from field notes and photographs. Scale character terminology follows Williams et al. (1995) and Köhler (2014). All measurements were taken with a digital caliper to the nearest 0.1 mm and the mean and standard deviation was estimated for each variable. Sex was determined by the presence of dewlap and hemipenes in males. Morphometric analysis. We used 23 morphometric traits recommended in anoles lizards (Lee 1980; Poe 2004, Williams et al. 1995; Köhler 2014) (abbreviations in parenthesis): snout-vent length (SVL) from the tip of snout to anterior margin of cloaca; tail length (TL) from the tip of intact tail to posterior margin of cloaca; head length (HL) from the tip of snout to anterior margin of ear; head width (HW) measured at the widest point of the head; jaw length (JL) from the anterior margin of rostrum to angle of jaw; interorbital distance (IoD) measured across the frontal bone (minimum distance between orbits); meatus Diameter (ED) maximum diameter of meatus; Meatus length (EL) maximum length of meatus; axilla-groin length (AGL) from posterior margin of arm at its insertion to anterior margin of leg at its insertion; internarial distance (InD) measured as the minimum distance between external nares viewed from above; Nose-face distance (NRD) distance from anterior margin of external nose to anterior margin of rostrum; meatus-jaw distance (EJL) from anterior margin of external auditory meatus to angle of jaw; narial diameter (ND) maximum diameter of nose in lateral view; snout length (SL) from anterior margin of orbit to tip of snout; interparietal length (IpL) maximum length of the scale; interparietal width (IpW)

214 · Zootaxa 4303 (2) © 2017 Magnolia Press GRISALES-MARTÍNEZ ET AL. maximum width of the scale; mental width (MW) maximum width of both scales as seen from below; humerus length (HuL) from the point at which the forelimb enters the body to the elbow; ulnae length (UlL) from the apex of the elbow to the centre of the wrist; femur length (FL) from the insertion in the body wall to knee; tibia length (TiL) from the knee to the center of the ankle on the ventral surface; foot length (FoL) from the ventral mid-point of the heel to the base of fourth toe; and fourth toe length (4tL) from the tip of the claw on fourth toe to the insertion into the foot (Table1). All measurements were log10-transformed. To remove the effect of body size, we calculated the residuals of the regressions of the log10-transformed morphological variables against log10-transformed SVL. The residual values were used as input in a principal component analysis including log10-transformed SVL based on a correlation matrix (Velasco & Herrel 2007). With the scores of the PCA we performed a discriminant analysis to estimate the probability of correct assignment of a specimen to a species. We conducted these analyses in R (R Core Team 2016) and STATISTICA v8.

TABLE 1. Arithmetic mean and associated standard deviation from selected morphometric characters in four species of Andean anoles. See text for abbreviations of measurements. Character Anolis urraoi Anolis mariarum Anolis antonii Anolis tolimensis Holotype Paratypes Males Females Males Females Males Females Males Femal (n = 21) (n = 17) (n = 9) (n = 10) (n = 7) (n = 6) (n = 5) e (n = 1) Mean±SD Mean±SD Mean±SD Mean±SD Mean±SD Mean±SD Mean±SD SVL 53.59 46.84±3.75 45.63±2.68 48.40±5.23 47.54±3.57 41.93±3.36 45.63±4.79 47.97±3.39 45.71 TL 13.95 12.19±0.88 11.85±0.71 13.12±1.33 12.76±0.76 10.56±1.86 12.88±2.46 12.47±0.76 12.95 HL 91.77 67.88±33.40 78.25±22.69 75.30±31.60 83.24±30.32 82.59±17.40 73.00±26.68 86.13±33.51 59.14 HW 8.57 6.77±1.55 7.15±0.49 7.87±0.70 7.32±1.86 6.71±0.53 7.38±0.74 7.60±0.49 7.84 JL 14.35 13.39±0.95 12.18±2.90 14.00±1.42 13.31±0.85 12.14±1.32 12.38±1.39 12.93±0.88 12.81 IoD 6.74 5.74±0.72 5.58±0.54 6.15±0.57 6.08±0.55 5.81±0.61 5.83±0.51 6.32±0.61 6.32 ED 0.82 0.88±0.15 0.81±0.12 0.74±0.12 0.91±0.22 0.89±0.19 1.05±0.31 0.97±0.08 1.06 EL 1.18 1.21±0.12 1.18±0.15 1.06±0.14 1.11±0.18 1.19±0.28 1.27±0.22 1.39±0.16 1.58 AGL 22.22 18.84±2.02 19.45±1.44 18.43±2.44 20.98±2.20 16.80±1.72 20.73±2.44 19.16±1.45 17.00 InD 2.08 1.85±0.21 1.84±0.17 2.04±0.25 2.16±0.27 1.74±0.24 1.87±0.20 2.17±0.33 2.21 NRD 0.73 0.66±0.15 0.72±0.23 0.97±0.21 0.98±0.17 0.47±0.22 0.73±0.27 1.53±0.15 1.17 EJL 2.09 2.14±0.25 2.29±0.34 2.30±0.43 2.26±0.21 1.84±0.29 2.02±0.52 2.24±0.25 2.52 ND 0.53 0.38±0.11 0.37±0.10 0.38±0.09 0.37±0.07 0.31±0.09 0.32±0.04 0.70±0.13 0.64 SL 6.81 5.63±0.50 5.36±0.57 6.22±0.68 6.14±0.59 5.24±0.92 5.65±0.63 5.28±0.32 5.48 IpL 1.81 1.27±0.41 1.37±0.44 1.22±0.20 1.45±0.26 1.34±0.24 1.60±0.28 0.91±0.06 0.90 IpW 0.92 0.89±0.33 0.84±0.31 0.85±0.29 0.88±0.17 0.81±0.12 0.83±0.18 0.32±0.08 0.39 MW 3.23 2.34±0.21 2.29±0.25 2.51±0.35 2.51±0.20 2.14±0.56 1.90±0.32 1.82±0.16 2.10 HuL 9.65 7.75±0.91 7.45±0.74 8.34±0.94 7.90±0.83 7.04±0.91 6.97±0.87 7.48±0.73 7.70 UIL 6.95 6.84±0.58 6.81±0.58 6.90±0.71 6.99±0.70 6.26±0.54 6.70±0.83 6.81±0.57 7.11 LF 13.33 12.08±0.87 11.69±0.76 12.39±1.54 11.11±0.72 10.23±1.34 11.23±0.94 10.61±0.53 10.29 TiL 13.45 12.11±0.69 11.85±0.85 11.38±1.51 11.10±1.01 11.44±1.20 11.88±0.83 11.61±0.53 11.30 FoL 18.55 16.13±0.94 15.84±1.07 15.33±1.65 14.92±0.72 14.31±1.63 15.00±0.90 15.35±0.94 14.34 4tL 10.85 9.18±0.70 8.98±0.77 8.63±0.81 8.24±0.68 7.53±0.92 8.20±0.64 8.44±0.70 8.74

Laboratory procedures. We amplified and sequenced the mitochondrial region ND2 for the four Andean species including the new taxon. Total genomic DNA was extracted from ethanol preserved tissues using the GeneJET Genomic DNA Purification kit (Thermo Fisher Scientific, Inc.). We amplified the ND2 region and the tRNAs Trp, Ala, Asn, Cys and Tyr using the primers Metf6 and COIr1 (Castañeda & de Queiroz 2011; Macey et al. 1997). PCR products were purified and sequenced at the Macrogen facilities in Korea (Macrogen, Inc.). Chromatographs were checked and sequences were edited using Geneious version 8.1.4 (http://www.geneious.com, Kearse et al. 2012). GenBank accession numbers for the sequences are provided in Appendix 2.

A NEW SPECIES OF ANDEAN ANOLIS Zootaxa 4303 (2) © 2017 Magnolia Press · 215 Phylogenetic analyses. We assembled a matrix including the four Andean species and the most related species to Anolis fuscoauratus D’Orbigny 1837 according to the phylogenetic hypothesis in Poe et al. (2017). We used Anolis auratus Daudin 1802 as the outgroup (Appendix 2). The ND2 region was aligned using MAFFT version 7 using the G-INS-i algorithm under default parameters (Katoh & Standley 2013). We inferred the best model of evolution using the Akaike Information criterion and a maximum likelihood tree. Both analyses were conducted using the program IQ-TREE (Nguyen et al. 2015). Nodal support was estimated using the ultrafast bootstrap method using 10000 pseudoreplicates (Minh et al. 2013). These support values are interpreted in a different way than the traditional bootstrap: while in a traditional bootstrap a value over 70% is considered a high support, a 95% ultrafast bootstrap value is considered high support (Minh et al. 2013).

Results

Description

Anolis urraoi sp. nov. (Figs. 1, 3, 4)

Proposed standard English name: Urrao anole Proposed standard Spanish name: Anolis de Urrao

Holotype. MHUA-R 12733; adult male, from departament of Antioquia, Urrao municipality, paddock on the banks of Río Penderisco: 6.314253, -76.138528, 1822 m, collected by B. Rendón-Valencia and F.A. Grisales-Martínez on 31 August, 2014 (Figs 1, 3; Table 1).

FIGURE 1. Anolis urraoi sp. nov. male holotype (MHUA-R 12733). Photograph by F. Grisales-Martínez.

216 · Zootaxa 4303 (2) © 2017 Magnolia Press GRISALES-MARTÍNEZ ET AL. FIGURE 2. Adult males of the Andean species of the Anolis fuscoauratus species group. A, A. aff. fuscoauratus, MHUA-R 12791, photo by Angelly Vasquez; B, A. tolimensis, MHUA-R 12770, photo by F.A. Grisales-Martínez; C, A. antonii, Bitaco, La Cumbre, Valle del Cauca, photo by W. Bolívar; and D, A. mariarum MHUA-R 12700, photo by M. Rivera-Correa.

Paratypes. n = 38: males = 21, females = 17 (all from Antioquia, Colombia. Table1). MHUA-R 12519-20-21, Urrao municipality, Corregimiento La Encarnación, vereda El Maravillo, Finca La Lucía, 6,51669, -76,1484, 2120

A NEW SPECIES OF ANDEAN ANOLIS Zootaxa 4303 (2) © 2017 Magnolia Press · 217 m, collected on 2012 by J.M. Daza; MHUA-R 12521, 12523, 12525, 12526, 12528, 12529, 12530, 12532, 12535, 12536, 12539, 12540, 12541, 12544, 12545, Urrao municipality, Corregimiento La Encarnación, vereda El Maravillo, 6.52133, -76.14022, 2156 m, collected on 2012 by J.M. Daza; MHUA-R 12731-32, Urrao municipality, in the urban area, paddock on the banks of river Penderisco, 6.314434, -76.138444, 1816 m, collected on 31 August, 2014 by B. Rendón-Valencia and F.A. Grisales-Martínez; CSJ 455, 467, 814, 819, 822-23, 837, 839, Urrao municipality, Las Orquideas National Park, vereda Calles, collected by M.A. Serna and H. Echeverri; CSJ 635; 703,815, 843, 848, 856, 858-59, 1028, 1074-75, Urrao municipality, La Magdalena, collected by M.A. Serna and H. Echeverri. Diagnosis. An small brown-greenish Anolis assigned to the Anolis fuscoauratus group by phylogenetic evidence presented in this study (see phylogenetic results) and by having the following combination of morphological characters described by Williams (1976) and Ayala & Williams (1988): 1) Head with small frontal depression and keeled scales not enlarged (similar in size to the dorsal scales); 2) small dorsal scales, uniform and usually keeled (smaller than ventral scales); 3) smooth ventral scales (sometimes with a low keeling); 4) broad and well-defined toes lamellae; 5) less than 20 lamellae on phalanges II and III of the fourth toe; and 6) round and slender tail without ridge.

FIGURE 3. Holotype of Anolis urraoi sp. nov. (MHUA-R 12733, adult male). A, dorsal; B, lateral; C, ventral view of head; D, detail of dorsal scales at mid-dorsum of body; E, detail of flank scales at mid-dorsum of body; and F, detail of ventral scales at mid-dorsum of body. Scale bar = 5 mm.

218 · Zootaxa 4303 (2) © 2017 Magnolia Press GRISALES-MARTÍNEZ ET AL. Because the Anolis fuscoauratus group is not recognized in the most comprehensive phylogeny to date (i.e., Poe et al. 2017), for our taxonomic account we compared the new taxon with species closely related or distributed in the same biogeographic regions (e.g., Central America, Pacific lowlands and the northern Andes). Anolis urraoi sp. nov. differs from other species in the A. fuscoauratus group from Central America by having a male dewlap bright orange anteriorly and light rose color on the posterior third or half. In contrast, males of Anolis elcopeensis Poe, Scarpetta & Schaad 2015, Anolis gruuo Köhler, Ponce, Sunyer & Batista 2007, Anolis carpenteri Echelle, Echelle & Fitch 1971 and Anolis polylepis Peters 1874 all have orange dewlap; Anolis kemptoni Dunn 1940 and Anolis pseudokemptoni Köhler, Ponce, Sunyer & Batista 2007 have red-orange anterior and pink posterior male dewlap; Anolis fortunensis Arosemena & Ibáñez 1993 has red anterior and orange posterior male dewlap; Anolis monteverde Köhler 2009 yellow ocher to orange yellow in the basal portion and reddish-orange in the distal portion of the male dewlap; Anolis altae Dunn 1930 with a more or less uniformly reddish-orange male dewlap; Anolis limifrons Cope 1862 with a dull white with a small basal orange blotch male dewlap, Anolis apletophallus Köhler & Sunyer 2008 with a uniformly dull white, almost uniformly orange male dewlap; Anolis tenorioensis Köhler 2011 with a dark red with brown blotches male dewlap. Furthermore, these species have a geographic distribution in the mid-highlands of lower Central America and A. urraoi sp. nov. is distributed in northwestern Andes in South America. Anolis urraoi sp. nov. is distinguished from the South America members of A. fuscoauratus group by male dewlap and meristic patterns. A. urraoi sp. nov. have a male dewlap bright orange anteriorly and light rose color on the posterior third or half (vs. A. tolimensis with solid reddish-orange male dewlap; A. antonii with a reddish- orange anterior and pink posterior male dewlap; A. mariarum with orange-red anterior and yellow posterior / orange-red anterior and pink posterior male dewlap; A. maculiventris with orange peripherally and red medially male dewlap; A. medemi with pink anterior and orange posterior male dewlap; A. trachyderma Cope 1875 with a reddish-orange with black scales male dewlap; A. fuscoauratus with solid pink male dewlap; A. bocourti Cope 1875 and A. scapularis Boulenger 1908 have a white male dewlap (the validity of this species has been questioned and it has been considered as a synonym of A. fuscoauratus, see Poe & Yañez-Miranda 2008) (Figure 4). Anolis urraoi sp. nov. have three to four scales between supraocular semicircles (vs. A. antonii one scale), 10 to 18 scales across the snout in the second canthal (vs. A. mariarum eight to 10 scales; A. tolimensis nine to 10 scales; A. maculiventris 10 to 14 scales), six or eight loreal rows (vs. A. antonii five); ventral scales slightly to strongly keeled (vs. ventral scales smooth to faintly keeled in A. tolimensis, A. antonii, and A. mariarum). Anolis urraoi sp. nov. is distributed in the northwestern Andes on the western slope of the Cordillera Occidental between 1700 and 2220 m meters above sea level. In contrast A. medemi is distributed in the Gorgona Island on the Pacific coast of Colombia; A. maculiventris in the Pacific lowlands and foothills of the Cordillera Occidental; A. fuscoauratus in the Magdalena river valley and the Amazonian region; A. trachyderma, A. bocourti, and A. scapularis in the Amazonian region. Additional characteristics from the Andean fuscoauratoid group are described in the table 2. Description of external morphology (holotype in parenthesis): Morphological dimensions are shown in Table 1. Head. Snout scales strongly keeled; keeling can be uni- or multicarinate; moderate prefrontal depression; shallow parietal depression. Circumnasal separated from the rostral scale by upper prenasal, lower prenasal; 6-7 (7) internasal scales; 6-8 (7) postrostral scales; distinct canthal ridge; usually 10-17 (11) scales between second canthals. Supraocular scales weakly keeled; one complete row of circumorbital scales to two rows of circumorbital scales with one incomplete; 3-4 (3) scales between supraorbital semicircles; 4-5 (4) scales between supraorbital semicircles and interparietal plate. Scales anterior to ear opening slightly larger than posterior; 6-8 (6) loreal scale rows; 40-65 (42) loreal scales; three subocular scales in narrow contact with three supralabial scales. Supralabials scales elongated with 6-7 (6) supralabial scales to level below center of eye; six (6) infralabial scales to level below center of eye; the first pair of sublabials is identical with the outer pair of postmentals; slightly enlarged outer postmental scales with 6-8 (6). Trunk. Dorsal scales keeled-conical; subimbricate scales with rounded posterior margins the 7-10 (9) median rows moderately enlarged; 80-106 (88) dorsal scales between levels of axilla and groin; lateral body scales homogeneous conical without axillary depression; ventral scales slightly to strongly keeled, subimbricate scales with mostly rounded posterior margins, some slightly mucronate; 58-71 (60) ventral scales between levels of axilla and groin.

A NEW SPECIES OF ANDEAN ANOLIS Zootaxa 4303 (2) © 2017 Magnolia Press · 219 Dewlap. Dewlap large-sized, the anterior insertion is below level of eye, the posterior insertion onto chest; lateral scales subequal to ventrals in 8-10 (8) rows descending posteriorly, each a single scale wide; edge scales small, imbricate, keeled, closely peaked (Figure 4). Limbs. Limb scales unicarinate dorsally, granular posteriorly and ventrally; supradigital scales strongly keeled; 13-16 (14) lamellae under phalanges II and III of fourth toe; subdigital pad is clearly dilated, while the width of the subdigital scales of the distal phalanx does not show dilatation.

FIGURE 4. Dewlap coloration in Andean anoles. A, Anolis urraoi sp. nov., paratype, MHUA-R 12732, photo by F.A. Grisales-Martínez; B, A. urraoi sp. nov., holotype, MHUA-R 12733, photo by F.A. Grisales-Martínez; C, A. urraoi sp. nov., paratype, MHUA-R 12541, photo by F.A. Duarte; D, A. fuscoauratus, QCAZ 8326, Pastaza, Ecuador, photo by M.R. Bustamante, FaunaWebEcuador; E, A. antonii, El Dovio, Valle del Cauca, photo by D. Alzate-Estrada; F, A. antonii, Yotoco, Valle del Cauca, photo by W. Bolívar; G, A. tolimensis, MHUA-R 12770, photo by F.A. Grisales-Martínez; H, A. mariarum MHUA-R 13033, photo by F.A. Grisales-Martínez; and I, A. mariarum MHUA-R 12730, photo by F.A. Grisales-Martínez.

Tail. Tail slender, cylindrical or very slightly compressed, somewhat swollen at the base in males, all scales keeled, median dorsal scales slightly enlarged; postcloacal scales not differentiated. Hemipenis. Preserved males did not have well everted hemipenis and detailed description of relevant characters could not be recovered. In general, the hemipenis in Anolis urraoi sp. nov. is small, tubular and slightly bifurcated distally. Color in life. Some specimens are brown with a black stripe on the back, while others have a greenish color. The colors are somewhat sexually dimorphic (see below).

220 · Zootaxa 4303 (2) © 2017 Magnolia Press GRISALES-MARTÍNEZ ET AL. Females: Head dark greenish brown to black; a brown or yellow crossbar between eyes sometimes present. Body brown or yellow-brown to yellowish or olive green, usually black or very dark brown middorsally, occasionally interrupted with brown spots; sides brown or yellow-brown, occasionally with darker vertical shadows or small rufous spots. In some females a slender light brown vertebral stripe is bordered laterally by thin dark brown lines extending from head to tail. Gular and belly regions white, usually maculate, with dark brown spots or striations. Legs brown, sometimes with narrow pale crossbands. Tail brown, usually with broad alternating dark brown and yellow brown bands, ventrally white on proximal third. Males: Head and body similar to females, more often greenish brown, black or dark brown middorsal region usually broader than in females, sometimes crossed with this greenish bands. Sides brown, tan or yellowish green, sometimes with small white spots. Gular and belly areas cream, infrequently spotted or striated with dark brown. Dewlap is bright orange anteriorly and light rose color on the posterior third or half, longitudinal rows of white scales.

TABLE 2. Comparison of morphological traits among species in the Andean Anolis fuscoauratus group. Character A. antonii 1 A. mariarum 2 A. tolimensis 3 A. urraoi4 Scales between 11T22T33T4 semicircles Scales between second Undescribed 8T10 9T10 10T18 canthals Loreal rows 5 5T76T76T8 Supralabials to below the 6T76T76T76T7 centre of the eye Gular scales Feebly keeled Feebly keeled Feebly keeled Edge scales small, imbricate, keeled, closely peaked Dorsal scales Dorsal scales small, Dorsal scales small, Dorsal scales small, Dorsal scales flat, keeled, becoming conical granules, the conical granules, the keeled-conical; gradually smaller median rows being median rows being subimbricate towards the sides, slightly enlarged and slightly enlarged and scales with where they are minute keeled, laterals becoming keeled, laterals rounded posterior and granular very small. becoming very small. margins the 7-10 median rows moderately enlarged.

Belly and chest scales Ventral scales larger Ventral scales much Ventral scales larger than Ventral scales than dorsals, flat, larger than dorsals, flat, dorsals, flat, larger than juxtaposed, smooth to subimbricate, cycloid, subimbricate, cycloid, dorsals, some faintly keeled smooth to faintly keeled. smooth. slightly mucronate, subimbricate, slightly to strongly keeled.

Dewlap male Reddish-orange Orange-red anterior and Solid reddish-orange Yellowish-orange anterior and pink yellow posterior/ anteriorly and posterior. Orange-red anterior and opaque pink on pink posterior. the posterior third or half. Lamellae under phalanges 16 15 to 16 13 to 16 13 to 16 II and III of fourth toe

1 Based on the description of A. antonii Boulenger 1908 and specimen photographs. 2 Based on the description of A. mariarum Barbour 1932 and fresh specimens from the type locality (see Appendix 1). 3 Based on fresh specimens from the type locality (see Appendix 1). 4 Based on series type.

A NEW SPECIES OF ANDEAN ANOLIS Zootaxa 4303 (2) © 2017 Magnolia Press · 221 TABLE 3. Loadings of the SVL and 22 traits corrected for body size (see main text for details) in the principal component analysis (PCA) for adult specimens of the four Andean species of the Anolis fuscoauratus species group: A. antonii, A. mariarum, A. tolimensis, and A. urraoi. Variable PC1 PC2 PC3 PC4 SVL -0.240 0.024 -0.037 0.009 TL -0.165 0.250 0.334 -0.534 HL -0.237 0.045 -0.009 0.055 HW -0.210 0.117 -0.057 0.157 JL -0.210 0.016 -0.121 -0.062 IoD -0.194 0.207 -0.248 0.219 ED -0.240 0.035 -0.024 0.032 EL -0.241 0.023 -0.035 0.021 AGL -0.166 0.163 0.525 -0.236 InD -0.208 0.244 -0.128 0.226 NRD -0.223 0.200 0.029 0.143 EJL -0.209 0.017 0.089 0.168 ND -0.226 0.100 0.023 0.259 SL -0.184 0.187 -0.143 -0.241 IpL -0.239 0.019 -0.004 0.005 IpW -0.239 0.012 -0.031 -0.008 MW -0.217 -0.058 -0.263 -0.140 HuL -0.175 -0.082 -0.417 -0.424 UIL -0.186 0.028 0.379 0.017 FL -0.182 -0.390 -0.134 -0.277 TiL -0.197 -0.328 0.244 0.265 FoL -0.180 -0.498 0.121 0.075 4tL -0.193 -0.432 0.070 -0.023 Cumulative Variance 0.732 0.786 0.822 0.850

Color in preservative. Preserved specimens dark brown or black middorsally (dark area broader in males), flanks with light brown, but in some few specimens, flanks are covered with a light orange or green (although this last condition is very rare). However, this green coloration in life is lost in preservative. Fore and hind legs may have light crossbars. No dark shoulder or occipital spot. Belly white or brownish white, darker toward sides, speckled (especially in females) with brown spots. Gular region in females white or white speckled with brown spots or vermiculations. Dewlap pale, often yellowish in anterior half, sometimes pale pink posteriorly, scale rows usually pigmented. Geographic distribution. Anolis urraoi sp. nov. is known from Urrao municipality, Antioquia department, in the northwestern Andes of Colombia between 1700 and 2220 m of elevation (Figure 5). Ecological Notes. Anolis urraoi sp. nov. is very common in the type locality. Specimens were collected mainly in open areas with shrubs and fences near human buildings, along sidewalks and roadways, and along the banks of the Penderisco river. The habitat is similar where other congeners are commonly found (e.g., A. mariarum and A. tolimensis). Males are commonly seen on bushes and stakes (up to 3 meters high) performing display, while females are usually elusive and occupying low perches. Individuals of the type series (MHUA-R 12731-32-33) were found between 10:00 and 11:00 in a sunny day (October 31, 2014) (Figure 6). Phylogenetic results. Anolis mariarum, A. antonii, and A. tolimensis form a monophyletic clade with a strong support (99%; Figure 7) related to A. altae from Costa Rica. By contrast, A. urraoi sp. nov. is more related to forms from the Pacific lowlands as A. medemi (Figure 7) and probably A. maculiventris (not included in this analysis). Also, this other clade is related with species from Central America (i.e., Anolis kemptoni and Anolis sp. JGP2014,

222 · Zootaxa 4303 (2) © 2017 Magnolia Press GRISALES-MARTÍNEZ ET AL. see Phillips et al. 2015). Although we did not have an extensive sampling within the large A. fuscoauratus group (see Poe et al. 2017 for a complete phylogeny of all known anole species), the apparent geographic disjunction between the sister species A. urraoi sp. nov. and A. medemi is most likely the result of lack of samples of species distributed in the Pacific lowlands of Colombia, Ecuador and Central America.

FIGURE 5. Distribution map of the species in the Anolis fuscoauratus group included in this study. S and M indicate sequenced specimens and measured specimens respectively.

Morphometric analysis. The PCA based on SVL and residual traits shown that Andean fuscoauratoid species tend to be grouped by body size (SVL) and shape traits (Figure 8). The loadings of each trait are shown in the Table 3. In the first PC axis, the SVL and ED exhibited the highest loads. In the second PC axis, the TL exhibited the highest load (Table 3). Although the overlap between all forms is very high, Anolis urraoi sp. nov. tend to separate in the morphospace from the rest of species in the second PC axis (hindlimb dimensions). The discriminant analysis revealed that specimens from A. urraoi sp. nov., A. mariarum, A. antonii, and A. tolimensis were assigned correctly to each species with a high probability (p-value > 0.5). Some specimens assigned tentatively to A. mariarum from Frontino National Park (at Western Cordillera from the Andes) seems to overlap strongly with A. urraoi sp. nov., A. antonii, and A. mariarum (Figure 8). Etymology. The specific name urraoi refers to the locality where the new species was found, the Urrao municipality, a town on the northwestern Andes in Antioquia.

Discussion

The taxonomy of Andean Anolis species from the Norops clade have been problematic for decades because its high

A NEW SPECIES OF ANDEAN ANOLIS Zootaxa 4303 (2) © 2017 Magnolia Press · 223 similarity in morphology and body coloration. In addition, even though dewlap coloration has been considered a very species-specific trait, some concerns rise as such coloration can converge to a similar pattern (Nicholson et al. 2007). Here, we provided, for the first time, an exhaustive examination of meristic, morphometric and molecular variation for the four Andean species: Anolis antonii, A. mariarum, A. tolimensis, and A. urraoi sp. nov. As geographic variation in molecular and morphological traits can obscure the real identity of species, we collected information in the type locality for all the species.

FIGURE 6. Habitat of Anolis urraoi sp. nov. on the banks of the Penderisco river, Urrao, Antioquia, Colombia.

Previous studies have shown that the phylogenetic status Anolis fuscoauratus group is controversial (Nicholson 2002; Poe et al. 2015; 2017). We found evidence that the “Andean” representatives of the A. fuscoauratus group do not form a monophyletic group (see also Poe et al 2017). Instead, one species (A. urraoi sp. nov.) is more related to a lowland species from the Pacific coast (A. medemi). According to our preliminary phylogenetic hypothesis and the biogeographic distribution, A. urraoi sp. nov. might be more related to other fuscoauratoids from the Pacific lowlands (e.g., A. maculiventris, not included here). Thus, we consider the phylogenetic position of A. urraoi sp. nov. as tentative, and more thorough sampling is necessary in particular in the Chocoan lowlands and the foothills of the northwestern Andes from Colombia and Ecuador. We found evidence supporting that A. antonii (from Valle del Cauca, Quindío, and Risaralda departments in Colombia) conforms a clade with A. tolimensis (endemic to the Cañon del Tolima, Tolima department in Colombia) and A. mariarum (only including the populations from the Central Andes in Antioquia department) (Figure 7, with a 99% ultrafast bootstrap value). In this study, we were able to include specimens from the type locality for all three species, therefore providing more evidence of species limits and geographic distribution of these forms. However, an extensive phylogeographic study is needed to better understand geographic limits of the different species and to uncover potential hidden lineages across the northern Andes. Recently, we discovered several specimens of the fuscoauratoid group from the Magdalena river valley that we were unable to assign to any known species (e.g., A. tolimensis or A. mariarum). With the molecular approach adopted here, we found that these three populations can be assigned to the species A. fuscoauratus (Figure 7).

224 · Zootaxa 4303 (2) © 2017 Magnolia Press GRISALES-MARTÍNEZ ET AL. FIGURE 7. Maximum likelihood tree (-lnL=-13314.977) obtained with IQ-TREE depicting the phylogenetic relationships in the Andean species of the Anolis fuscoauratus species group. Inference based on 1465 characters of the ND2 gene and intervening regions. Nodal support was estimated using the ultrafast bootstrap method using 10000 pseudoreplicates (Minh et al., 2013).

A NEW SPECIES OF ANDEAN ANOLIS Zootaxa 4303 (2) © 2017 Magnolia Press · 225 These three records are the first ones to be reported for A. fuscoauratus with a trans-Andean distribution (Figure 5). For decades, trans- and cis- Andean lowland fauna has been considered very distinct. For Anoline fauna, this is almost a rule with the only exception of A. auratus that is distributed from Costa Rica to (Avila-Pires 1995). There are many snake species and other amphibians with a widespread distribution and our recent work effort on the Magdalena river valley in Antioquia, more species of amphibians and previously known only from the Amazonian side, are being added to the trans-Andean fauna (Atractus occipitoalbus Marín et al. 2017; Cochranella resplendens Molina-Zuluaga et al. 2017). Therefore, our finding of A. fuscoauratus in the Magdalena river valley is not a surprise and we suspect that more species with similar distribution patterns will be unhidden once we put more effort in fieldwork, molecular and morphological approaches in this region. The extreme difficulty in Andean anoles’s taxonomy is mostly due to the high similarity in meristic traits, the reliance mostly on adult males and the unknown intraspecific variation in dewlap coloration. In addition, preserved specimens lose pigmentation making even more difficult to assign them unambiguously to a species. A similar challenge is found in other fuscoauratoid taxa from Central America (A. kemptoni, A. altae; Ponce & Köhler 2008; Köhler 2009, 2011) and the Greater Antilles anoles (A. distichus; Glor & Laport 2012). Accordingly, we suggest that in future taxonomic studies it is necessary to include type localities and implement genetic data combined with better morphological quantitative analyses in this highly diverse but taxonomically complex Neotropical lineage.

FIGURE 8. PCA plot of morphometric measurements from specimens of Anolis urraoi sp. nov. (red squares), A. mariarum (magenta circles), A. antonii (blue triangles), A. tolimensis (green diamonds) and some individuals tentatively assigned to A. mariarum (from Western Cordillera at Frontino National Park; black circles). PCA was performed with SVL (snout-vent length) and 22 morphological traits corrected for size (main text for details).

226 · Zootaxa 4303 (2) © 2017 Magnolia Press GRISALES-MARTÍNEZ ET AL. Acknowledgements

Fieldwork and collecting permits were funded by Instituto Alexander von Humboldt and Universidad de Antioquia under Proyecto Delimitación de Páramos y Humedales (contract 005–13–014). We thank the MHUA and CSJ collections for specimen loan and for providing their facilities. We thank B.E. Rendón, J. Fang, F. Duarte, C. Jiménez, N. Cala, Y. Tolosa and M. Martínez for their assistance in the field. J. Sunyer helped with German translation of Anolis descriptions. D. Alzate-Estrada, M. Rivera, M.R. Bustamante and A. Vásquez whom provided life photos. We thank J.B. Losos and J. Rosado from the Museum of Comparative Zoology (Harvard University) for gently answering questions related with unpublished writings from E. E. Williams. We are very grateful to the people from Urrao for their kindness and strength, despite of being a town affected by decades of civil conflict.

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APPENDIX 1. Specimens of the Anolis fuscoauratus group examined

Anolis antonii: COLOMBIA: RISARALDA: Apia, Vereda Agua Linda, Parque Municipal Natural Agualinda (5.115, -75.927): CZPD 3996; Santa Rosa de Cabal, Vereda La Paloma, Finca La Bonita (4.854, -75.585): CZPD 4002; VALLE DEL CAUCA: Darien, Lago Calima, Finca La Tesalia (3.892, -76.467): CZPD 3998; QUINDÍO: Filandia, Parque Regional Natural Barbas- Bremen, Fragmento La Chena (4.681639, -75.648861; 1856 m) CZPD 3993; Filandia, Parque Regional Natural Barbas- Bremen, fragmento al final del camino de Lusitania (4.702972, -75.649361; 1874 m): CZPD 4000.

Anolis mariarum—COLOMBIA: ANTIOQUIA: San Pedro, Vereda La Lana (6.44780, -75.60720; 2600 m): MHUA-R 11618- 19-20-21-22; San Pedro, Vereda El Tambo (6.41861, -75.59861; 2587 m): MHUA-R 11819, 11824, 11854-55, 11860, 11900, 12178, 12203-04, 12206; Anorí, Vereda El Retiro, Finca Chaquiral (6.97938, -75.12973; 1752 m): CD 3994-95, 3997; Rionegro, Vereda Santa Bárbara, Finca El Carmelo (6.210208, -75.372593; 2140 m): MHUA-R 12730.

Anolis tolimensis—COLOMBIA: TOLIMA: Ibagué, Cañón del Combeima, Vereda Llanitos (4.488334, -75.282444; 1551): MHUA-R 12769-70-71; Ibagué, Cañón del Combeima, Vereda Llanitos (4.488307, -75.282424; 1563): MHUA-R 12772-73; Ibagué, Cañón del Combeima, Vereda Juntas (4.551389, -75.327639; 1910): MHUA-R 12774.

APPENDIX 2. Terminals and GenBank accession numbers for the ND2 locus used in this study. Species Voucher Locality Accession Anolis altae Costa Rica AY909735 Anolis antonii CZPD 5006 Filandia, Caldas, Colombia MF449477 Anolis antonii CZPD 5007 Filandia, Caldas, Colombia MF449481 Anolis antonii CZPD 5008 Filandia, Caldas, Colombia MF449482 Anolis antonii CZPD 5010 Yotoco, Valle del Cauca, Colombia MF449483 Anolis antonii CZPD 5011 Santuario, Risaralda, Colombia MF449478 Anolis antonii CZPD 4077 Mistrató, Risaralda, Colombia MF449484 Anolis antonii CZPD 4998 Mistrató, Risaralda, Colombia MF449485 Anolis antonii CZPD 3675 Apia, Risaralda, Colombia MF449479 Anolis antonii CZPD 3996 Apia, Risaralda, Colombia MF449480 Anolis auratus AY909740 Anolis cupreus AY909750 Anolis fuscoauratus MHUAR12433 San Carlos, Antioquia, Colombia MF449498 Anolis fuscoauratus MHUAR12493 Norosí, Bolívar, Colombia MF449499 Anolis fuscoauratus MHUAR12496 Norosí, Bolívar, Colombia MF449500 ...... continued on the next page

A NEW SPECIES OF ANDEAN ANOLIS Zootaxa 4303 (2) © 2017 Magnolia Press · 229 APPENDIX 2. (Continued) Species Voucher Locality Accession Anolis fuscoauratus H0805 Porto Velho, Rondonia, Brazil KX760528 Anolis fuscoauratus LSUMZH12538 Sucumbios, Ecuador AF337789 Anolis fuscoauratus LSUMZH12545 Sucumbios, Ecuador AF337788 Anolis fuscoauratus LSUMZH13566 Acre, Brazil AF337786 Anolis fuscoauratus LSUMZH13801 Acre, Brazil AF337787 Anolis fuscoauratus LSUMZH14094 Amazonas, Brazil AF337790 Anolis fuscoauratus LSUMZH14327 Para, Brazil AF337791 Anolis fuscoauratus LSUMZH15471 Rondonia, Brazil AF337792 Anolis fuscoauratus PEU488 Ilheus, Bahia, Brazil KX760529 Anolis humilis KJ954107 Anolis isthmicus AY909762 Anolis kemptoni AY909770 Anolis mariarum MHUAR11077 Caldas, Antioquia, Colombia MF449486 Anolis mariarum MHUAR11985 Marinilla, Antioquia, Colombia MF449489 Anolis mariarum MHUAR11998 Girardota, Antioquia, Colombia MF449488 Anolis mariarum MHUAR12069 Santo Domingo, Antioquia, Colombia MF449492 Anolis mariarum MHUAR12659 Santa Rosa de Osos, Antioquia, Colombia MF449495 Anolis mariarum MHUAR12678 Rionegro, Antioquia, Colombia MF449490 Anolis mariarum MHUAR12700 Barbosa, Antioquia, Colombia MF449493 Anolis mariarum MHUAR12730 Rionegro, Antioquia, Colombia MF449494 Anolis mariarum MHUAR12734 Don Matías, Antioquia, Colombia MF449496 Anolis mariarum MHUAR12737 Santo Domingo, Antioquia, Colombia MF449491 Anolis mariarum MHUAR12804 Caldas, Antioquia, Colombia MF449487 Anolis medemi Isla Gorgona, Cauca, Colombia KJ953921 Anolis poecilopus AY909771 Anolis polylepis AY909772 Anolis quaggulus KJ953945 Anolis sericeus AY909778 Anolis sp. JGP2014 KJ953923 Anolis tolimensis MHUAR12774 Ibagué, Tolima, Colombia MF449497 Anolis townsendi KJ953922 Anolis trachyderma AF294285 Anolis tropidogaster AY909782 Anolis tropidonotus AY909783 Anolis urraoi MHUAR12517 Urrao, Antioquia, Colombia MF449501 Anolis urraoi MHUAR12523 Urrao, Antioquia, Colombia MF449502 Anolis urraoi MHUAR12525 Urrao, Antioquia, Colombia MF449504 Anolis urraoi MHUAR12528 Urrao, Antioquia, Colombia MF449503 Anolis urraoi MHUAR12731 Urrao, Antioquia, Colombia MF449506 Anolis urraoi MHUAR12732 Urrao, Antioquia, Colombia MF449507 Anolis urraoi MHUAR12733 Urrao, Antioquia, Colombia MF449505

230 · Zootaxa 4303 (2) © 2017 Magnolia Press GRISALES-MARTÍNEZ ET AL.

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