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DNA Barcoding of an Assembly of Montane Andean Butterflies (Satyrinae): Geographical Scale and Identification Performance

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DNA Barcoding of an Assembly of Montane Andean Butterflies (Satyrinae): Geographical Scale and Identification Performance Neotrop Entomol DOI 10.1007/s13744-016-0481-z SYSTEMATICS, MORPHOLOGY AND PHYSIOLOGY DNA Barcoding of an Assembly of Montane Andean Butterflies (Satyrinae): Geographical Scale and Identification Performance 1,2 2 2 2,3 2 4 5 MA MARÍN ,ICCADAVID ,LVALDÉS ,CFÁLVAREZ ,SIURIBE ,RVILA ,TWPYRCZ 1Depto de Biologia Animal, Instituto de Biologia, Univ Estadual de Campinas – UNICAMP, Campinas, SP , Brazil 2Univ Nacional de Colombia, Sede Medellín, Grupo de Investigación en Sistemática Molecular, Medellín, Colombia 3Corporación Universitaria Lasallista, Antioquia, Colombia 4Instituto de Biología Evolutiva (CSIC-UPF), Barcelona, Spain 5Zoological Museum, Jagiellonian Univ, Kraków, Poland Keywords Abstract Pronophilina, Morpho, Forsterinaria, DNA barcoding is a technique used primarily for the documentation and mitochondrial DNA, molecular taxonomy, identification of biological diversity based on mitochondrial DNA se- andean cloud forest, community ecology quences. Butterflies have received particular attention in DNA barcoding Correspondence studies, although varied performance may be obtained due to different MA Marín, Depto de Biologia Animal, Instituto de Biologia, Univ Estadual de scales of geographic sampling and speciation processes in various groups. Campinas – UNICAMP, Rua Monteiro Lobato, The montane Andean Satyrinae constitutes a challenging study group for 255 - Cidade Universitária Zeferino Vaz - Barão taxonomy. The group displays high richness, with more of 550 species, and Geraldo, CEP, Campinas, SP 13083-970, Brazil; [email protected] remarkable morphological similarity among taxa, which renders their iden- tification difficult. In the present study, we evaluated the effectiveness of Edited by Alberto S Corrêa – ESALQ/USP DNA barcodes in the identification of montane Andean satyrines and the Received 15 June 2016 and accepted 28 effect of increased geographical scale of sampling on identification perfor- December 2016 mance. Mitochondrial sequences were obtained from 104 specimens of 39 species and 16 genera, collected in a forest remnant in the northwest * Sociedade Entomológica do Brasil 2017 Andes. DNA barcoding has proved to be a useful tool for the identification of the specimens, with a well-defined gap and producing clusters with unambiguous identifications for all the morphospecies in the study area. The expansion of the geographical scale with published data increased genetic distances within species and reduced those among species, but did not generally reduce the success of specimen identification. Only in Forsterinaria rustica (Butler, 1868), a taxon with high intraspecific varia- tion, the barcode gap was lost and low support for monophyly was ob- tained. Likewise, expanded sampling resulted in a substantial increase in the intraspecific distance in Morpho sulkowskyi (Kollar, 1850); Panyapedaliodes drymaea (Hewitson, 1858); Lymanopoda obsoleta (Westwood, 1851); and Lymanopoda labda Hewitson, 1861; but for these species, the barcode gap was maintained. These divergent lineages are nonetheless worth a detailed study of external and genitalic morphology variation, as well as ecological features, in order to determine the poten- tial existence of cryptic species. Even including these cases, DNA barcoding performance in specimen identification was 100% successful based on monophyly, an unexpected result in such a taxonomically complicated group. Marín et al Introduction 2011,Ashfaqet al 2013,Wilsonet al 2013,Dincă et al 2011, 2015, Yang et al 2015), and a total of 148,306 DNA barcodes Andean Satyrinae are available for named butterflies specimens (Papilionoidea) in the Barcode of Life Database (BOLD Systems v3, accessed In the Neotropics, the subfamily Satyrinae accounts for more on October 6, 2016). However, some studies have shown than 1200 known species in five tribes (Morphini, Brassolini, that DNA barcodes are not completely accurate when iden- Haeterini, Melanitini, and Satyrini). Two Satyrini subtribes en- tifying specific taxonomical groups. Elias et al (2007), report- compass most of the species: Euptychiina, with more than 400 ed in Ithomiini (Danainae) that only 77% of species can be species, is a group of mostly lowland or premontane butterflies precisely identified using the barcode data at local scale (Viloria 2003), particularly diversified in the basin of the Amazon, (21 km2), while Wiemers & Fiedler (2007) reported 84% of Atlantic Forest, and the foothills of the Andes, and Pronophilina, accurately identified Polyommatinae (Lycaenidae) at a conti- more diverse in the highlands, is the richest group of montane nental scale. butterflies with over 550 described species (Lamas et al 2004), Dasmahapatra et al (2010) demonstrated that deep ge- and presents the greatest diversity in the tropical Andes. netic divergences detected with mtDNA barcoding in the Montane satyrines display high morphological similarity genus Mechanitis Fabricius, 1807 (Ithomiini), were not always among congeneric species (Forster 1964). For example, in reflected in the nuclear genome and suggested the use of Euptychiina, the genus Forsterinaria Gray, 1973 the only nuclear genes as a check step when mtDNA barcoding gives strictly montane within the subtribe, presents a demanding unexpected results. However, other studies supported the taxonomy (Zubek et al 2014). Its species show little differ- effectiveness of DNA barcoding for attribution of specimens ence in wing pattern and even the genitalia provide few to species, with an accuracy between 90–100% (Lukhtanov diagnostic characters for the immediate segregation of some et al 2009,Pradoet al 2011,Ashfaqet al 2013,Wilsonet al allopatric or sympatric species (Zubek & Pyrcz 2011). In some 2013,Dincă et al 2011, 2015), and its usefulness in the study Pronophilina, the situation is similar, particularly notable in of species complexes (Hebert et al 2004, Cong & Grishin diverse genera as Pedaliodes Butler, 1867; Eretris Thieme, 2014, Seraphim et al 2014). The variable performance of 1905; and Manerebia Staudinger, 1897. These exhibit a re- DNA barcoding has been attributed to factors such as sam- markable external similarity among many species, which can pling, geographic scale, time divergence among species, mi- only be identified with certainty through dissection, and this tochondrial introgression, and dominant mode of speciation fact has led to much confusion in the literature and resulted (Moritz & Cicero 2004,Eliaset al 2007, Wiemers & Fiedler in a significant underestimation of their taxonomic diversity 2007,Bergstenet al 2012, Talavera et al 2013). Interestingly, (Pyrcz et al 2006). DNA barcode libraries based on regional sampling may still Additionally, montane satyrines present an intricate alti- be effective at much wider geographic scales (Huemer et al tudinal distribution. Pronophilina butterflies occur predomi- 2014). Without a cause that fully explains the variability in nantly in high elevation cloud forests near or within the the performance of DNA barcoding, it is necessary to test its forest-paramo ecotone, but they are distributed in narrow utility for different taxa, and under different ecological and bands of altitude (Adams 1985, Pyrcz & Wojtusiak 2002, sampling conditions. Pyrcz et al 2009, Casner & Pyrcz 2010, Viloria et al 2010, Neotropical Satyrinae constitute an interesting model Pyrcz & Garlacz 2012,Marínet al 2015) and demonstrate a group for testing the performance of DNA barcoding because large percentage of endemic species, frequently confined to of high diversity and notable morphological stasis. However, single massifs (Pyrcz & Rodríguez 2007, Pyrcz et al 2013, and in contrast with other butterflies groups, montane 2016). Within each part of the Andes, lower-elevation species Andean satyrines have received little attention in molecular with broad geographic ranges are replaced by higher-eleva- studies (e.g., Casner & Pyrcz 2010). Accordingly, in the pres- tion, narrowly distributed congeners. The result is a stair-step ent study, we evaluated the effectiveness of DNA barcodes distribution in mountain sides with unique species composi- on the identification of montane Andean satyrines and the tion in adjacent regions of an extended mountain chain or in effect of increased geographical sampling scale on the per- nearby cordilleras (Adams 1985,Pyrczet al 1999, Casner & formance of this methodology. Pyrcz 2010). DNA Barcoding in Butterflies Material and Methods Butterflies have been widely used in DNA barcoding studies Specimens sampling (Hebert et al 2004, Elias et al 2007,Janzenet al 2009, Linares & Soto-Calderón 2009,Lukhtanovet al 2009,Silva- Butterflies were collected in a forest remnant of 51.71 km2 Brandão et al 2009, Dasmahapatra et al 2010,Pradoet al close to Medellín city in the Colombian Central Cordillera DNA Barcoding of Andean Satyrinae of the Andes (6°05′–6°13′N/75°39′–75°43′W), from March 2011 Analysis of genetic variability to February 2012 at 2500–2890 m. In this area, maximum annual rainfall is approximately 3000 mm (Corantioquia Pairwise distances were calculated in the software MEGA 5.2 2004, Hermelin 2007). According to Holdridge (1967), this life (Tamura et al 2011) using the uncorrected p distance model zone corresponds to montane rain forest and lower montane according to Collins et al (2012) and Srivathsana and Meiera wet forest. (2012), remaining analyses were conducted in the R package External morphology was used to examine and iden- Spider (Brown et al 2012). For analytical purposes, a distance tify collected specimens,
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