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Use of Species Delimitation Approaches to Tackle the Cryptic Diversity of an Assemblage of High Andean Butterflies (Lepidoptera: Papilionoidea)

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Use of Species Delimitation Approaches to Tackle the Cryptic Diversity of an Assemblage of High Andean Butterflies (Lepidoptera: Papilionoidea) Genome Use of species delimitation approaches to tackle the cryptic diversity of an assemblage of high Andean butterflies (Lepidoptera: Papilionoidea) Journal: Genome Manuscript ID gen-2020-0100.R2 Manuscript Type: Article Date Submitted by the 22-Jan-2021 Author: Complete List of Authors: Marín, Mario Alejandro; Universidade Estadual de Campinas Instituto de Biologia, Biologia Animal; Universidad Nacional de Colombia Sede Medellin, Grupo de Investigación en Sistemática Molecular López-Rubio,Draft Andrés; Universidad Nacional de Colombia Sede Medellin, Grupo de Investigación en Sistemática Molecular Clavijo, Alejandra; Universidad Nacional de Colombia Sede Medellin, Grupo de Investigación en Sistemática Molecular Pyrcz, Tomasz; Uniwersytet Jagielloński w Krakowie, Entomology Department; Uniwersytet Jagielloński w Krakowie, Natural Sciences Education Centre Freitas, Andre; Universidade Estadual de Campinas, Departamento de Biologia Animal, Instituto de Biologia Uribe, Sandra Inés; Universidad Nacional de Colombia Sede Medellin, Grupo de Investigación en Sistemática Molecular Álvarez, Carlos Federico; Universidad Nacional de Colombia Sede Medellin, Grupo de Investigación en Sistemática Molecular Keyword: ABGD, DNA barcode, GMYC, PTP, Satyrinae Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : © The Author(s) or their Institution(s) Page 1 of 39 Genome 1 Use of species delimitation approaches to tackle the cryptic diversity of an assemblage of 2 high Andean butterflies (Lepidoptera: Papilionoidea) 3 4 Mario Alejandro Marín1,2*, Andrés López-Rubio2, Alejandra Clavijo2, Tomasz Wilhelm 5 Pyrcz3,4, André Victor Lucci Freitas1,5, Sandra Inés Uribe2, and Carlos Federico Álvarez2 6 7 1 Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de 8 Campinas, São Paulo (SP), Brazil. 9 2 Grupo de Investigación en Sistemática Molecular, Universidad Nacional de Colombia, 10 Medellín, Antioquia, Colombia. 11 3 Entomology Department, Institute of Zoology and Biomedical Research, Jagiellonian 12 University, Gronostajowa, Kraków, Poland.Draft 13 4 Nature Education Centre, Jagiellonian University, Gronostajowa, Kraków, Poland. 14 5 Museu da Biodiversidade, Instituto de Biologia, Universidade Estadual de Campinas, São 15 Paulo, Brazil. 16 17 Mario Alejandro Marín 18 Corresponding author: [email protected] 19 20 21 22 23 24 25 1 © The Author(s) or their Institution(s) Genome Page 2 of 39 26 Abstract 27 Cryptic biological diversity has generated ambiguity in taxonomic and evolutionary studies. 28 Single-locus methods and other approaches for species delimitation are useful for addressing 29 this challenge, enabling the practical processing of large numbers of samples for identification 30 and inventory purposes. This study analyzed one assemblage of high Andean butterflies using 31 DNA barcoding and compared the identifications based on the current morphological 32 taxonomy with three methods of species delimitation (automatic barcode gap discovery, 33 generalized mixed Yule coalescent model, and Poisson tree processes). Sixteen potential 34 cryptic species were recognized using these three methods, representing a net richness 35 increase of 11.3% in the assemblage. A well-studied taxon of the genus Vanessa, which has a 36 wide geographical distribution, appeared with the potential cryptic species that had a higher 37 genetic differentiation at the local levelDraft than at the continental level. The analyses were useful 38 for identifying the potential cryptic species in Pedaliodes and Forsterinaria complexes, which 39 also show differentiation along altitudinal and latitudinal gradients. This genetic assessment 40 of an entire assemblage of high Andean butterflies (Papilionoidea), provides baseline 41 information for future research in a region characterized by high rates of endemism and 42 population isolation. 43 44 Key words: ABGD, DNA barcode, GMYC, PTP, Satyrinae, Vanessa 45 46 47 48 49 50 2 © The Author(s) or their Institution(s) Page 3 of 39 Genome 51 Introduction 52 Cryptic biological diversity has generated ambiguity in taxonomic and evolutionary studies 53 (Struck et al. 2018). This can be described as a problem of species delimitation, with two or 54 more distinct “lineages” that have been previously classified as one based on morphological, 55 ecological, distributional, ethological, or genetic similarity. This could represent a substantial 56 amount of biodiversity, the knowledge of which is essential for understanding evolutionary 57 processes and patterns of ecosystem functioning, thereby aiding nature conservation (Bickford 58 et al. 2007; Trontelj and Fišer 2009; Dincǎ et al. 2011). The magnitude of these hidden 59 species remains unknown, especially in diversified groups of relatively poorly explored 60 tropical regions (Funk et al. 2012). Several factors have generated an increasing interest in the 61 study of the cryptic diversity (Espíndola et al. 2016): (1) Conservation efforts on a regional 62 scale are often determined by species richnessDraft and endemism, and the identification of hidden 63 species is critical for estimating these parameters (Bickford et al. 2007; Espíndola et al. 2016; 64 Delić et al. 2017); (2) The discovery of cryptic biological diversity aids in establishing of 65 evolutionary significant units for conservation (Beheregaray and Caccone 2007); (3) The 66 understanding of anthropogenic biotic changes, invasions, and ecosystem health depends on 67 the knowledge of all species involved (Espíndola et al. 2016); and (4) The discovery of 68 cryptic diversity connects the study of taxonomy and phylogenetic patterns with ecosystem 69 functioning, evolutionary processes, and macroevolutionary trends (Struck et al. 2018). Thus, 70 it is necessary to intensify research beyond the phenomenological level of exploration and 71 incorporate further knowledge on cryptic species into biodiversity science (Fišer et al. 2018). 72 Cryptic diversity has been poorly considered in ecological and evolutionary theories 73 (Beheregaray and Caccone 2007). Single-locus methods used in species delimitation have 74 proven to be useful for the study of numerous samples, as they aid identification and 75 inventory of specimens, characterization and comparison of communities, evaluation of 3 © The Author(s) or their Institution(s) Genome Page 4 of 39 76 genetic variability, and understanding of the interactions among species within an ecosystem 77 (Craft et al. 2010; Kaartinen et al. 2010; Krishnamurthy and Francis 2012; Delabye et al. 78 2019). In Lepidoptera, the most used gene region for specimen identification and species 79 discrimination is the 5’-end of the mitochondrial cytochrome oxidase subunit I (COI) (revised 80 by Silva- Brandão et al. 2009), a fragment of 648 bp commonly referred to as the “DNA 81 barcode” region. Initially proposed by Hebert et al. (2003) as a standardized genetic marker 82 for Lepidoptera, the DNA barcode has been widely used to identify and inventory specimens 83 of particular taxonomic groups or regions (Lukhtanov et al. 2009; Sourakov and Zakharov 84 2011; Wilson et al. 2013; Huemer et al. 2014; Yang et al. 2016; Zenker et al. 2016; Ashfaq et 85 al. 2017; Lavinia et al. 2017; Marín et al. 2017; Zahiri et al. 2017). The effectiveness of this 86 method has enabled different usages in evolutionary and ecological studies, such as 87 comparing communities (Brehm et al.Draft 2016; Zenker aet al. 2016; Delabye et al. 2019), 88 evaluating the genetic variability within species (Linares et al. 2009; Craft et al. 2010; 89 Escalante et al. 2010; Dapporto et al. 2019), identifying the interactions among species within 90 an ecosystem (Baker et al. 2016; Rytkönen et al. 2019), determining the similarities and 91 differences within species complexes (Dumas et al. 2015; Pfeiler and Nazario-Yepiz 2020), 92 and in integrative phylogeographic studies on wide geographic scale (Dapporto et al. 2019). 93 In the tropical Andes cryptic species have frequently been reported in different taxa 94 such as birds (Rheindt et al. 2013; Mendoza et al. 2016; Krabbe et al. 2020), amphibians 95 (Kieswetter and Schneider 2013; Guarnizo et al. 2015), and mammals (Giarlia et al. 2014). 96 Diversified groups of butterflies such as the subfamily Satyrinae (Nymphalidae), the genus 97 Catasticta (Pieridae), and the family Lycaenidae, are recognized for their cryptic diversity and 98 restricted distribution, particularly in isolated massifs and at high altitudes (Pyrcz 2004; Pyrcz 99 and Rodríguez 2007; Prieto and Vargas 2016). This pattern of distribution and richness of 100 species is attributed to complex montane topography resulting in high species turnover, which 4 © The Author(s) or their Institution(s) Page 5 of 39 Genome 101 is promoted and maintained for both elevationl and allopatric replacement (Krabbe et al. 102 2020). Elevational replacement means that different species occupy distinct altitudinal zones 103 with habitat bands driven by temperature and precipitation gradients (Pyrcz and Wojtusiak 104 2002; Pyrcz et al. 2009; Casner and Pyrcz 2010; Pyrcz and Garlacz 2012), whereas allopatric 105 replacement has closely related species occupying similar elevations isolated from each other 106 by geographic barriers (Pyrcz et al. 2006; Pyrcz and Rodríguez 2007; Casner and Pyrcz 107 2010). This high species turnover, together with the recent radiation of many Andean butterfly 108 clades (Casner and Pyrcz 2010; Matos-Maraví et al. 2013; De Silva et al.
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