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Integrative Taxonomy Reveals Cryptic Amazonian Species of Pristimantis (Anura: Strabomantidae)

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Integrative Taxonomy Reveals Cryptic Amazonian Species of Pristimantis (Anura: Strabomantidae) Zoological Journal of the Linnean Society, 2009, 155, 97–122. With 9 figures Integrative taxonomy reveals cryptic Amazonian species of Pristimantis (Anura: Strabomantidae) JOSÉ M. PADIAL and IGNACIO DE LA RIVA* Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales, CSIC. C/ José Gutiérrez Abascal 2, 28006 Madrid, Spain Received 6 June 2007; accepted for publication 9 October 2007 Hypotheses on the taxonomic status of two Bolivian Pristimantis with taxonomic problems are assessed by an integrative taxonomic approach that integrates three independent lines of evidence: external morphology, prezy- gotic reproductive barriers (advertisement calls) and reciprocal monophyly (phylogenetic analyses of partial 16S mtDNA sequences). Central Andean Bolivian populations previously assigned to either P. peruvianus or P. dundeei, and lowland Amazonian populations from southern Peru and northern Bolivia previously considered P. peruvianus do not correspond to these species. Indeed, multivariate analyses of qualitative and quantitative morphological and bioacoustic characters, and phylogenetic analyses support the hypothesis that they represent different, previously unknown, cryptic lineages. They are herein described as new species. The former is a sibling species of P. fenestratus that inhabits the Amazonian and semideciduous forests of the Andean foothills in central Bolivia. The latter is sibling to the Andean species P. danae and is parapatric to it in the Amazonian lowland forests and adjacent foothills of northern Bolivia, southern Peru and adjacent Brazil. Most species of Neotropical frogs, and especially Pristimantis, have been described by using external qualitative morphological characters only. An extended integrative taxonomic approach, as exemplified herein, may lead to the discovery of many other cryptic and sibling lineages that would increase the species numbers of tropical areas. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 97–122. ADDITIONAL KEYWORDS: Andes – bioacoustics – mtDNA – new species. INTRODUCTION spite of the high rate of species discovery (Padial & De la Riva, 2006) and current conservation concern The Amazonian versant of the Andes and adjacent (Stuart et al., 2004). Most species are discovered by lowlands house one of the most diverse habitats of the means of standard exploration of remote or scarcely world (Myers et al., 2000), with National Parks such explored areas or through the revision of museum as Manu (Peru) or Madidi (Bolivia) as symbols of the specimens. In other words, most newly described preservation of the richest biodiversity hotspots. species represent quite obvious divergent lineages Among vertebrates, amphibians show high levels of evidenced by differences in qualitative morphological diversity and endemicity in these areas (Köhler, characters. The application of bioacoustics (e.g. Heyer, 2000a). Several Peruvian and Bolivian species are García-López & Cardoso, 1996; Angulo, Cocroft & today described and named every year both from the Reichle, 2003; Padial et al., 2008b) and molecular Andes (e.g. Padial, Chaparro & La Riva, 2006, 2007b; phylogenetics (e.g. Parra-Olea, García-París & Wake, Duellman & Lehr, 2007; Lehr & Duellman, 2007) and 2004; Fouquet et al., 2007; Lehtinen et al., 2007) to from the Amazonian lowlands (e.g. Moravec, Aparicio tropical taxonomy opens the door to new frontiers of & Köhler, 2006; Lehr, Torres & Suárez, 2007). data exploration that may potentially increase the rate However, these areas are still very poorly known in of species discovery. Indeed, cryptic and sibling species hidden to the eye of the classical taxonomist may be much more abundant in nature than expected *Corresponding author. E-mail: [email protected] (Bickford et al., 2007) both across taxa and across © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 97–122 97 98 J. M. PADIAL and I. DE LA RIVA geographical regions (Pfenninger & Schwenk, 2007). interbreeding, etc.) are now considered contingent If this is true also for amphibians, the number of, properties that represent thresholds crossed by diverg- for example, Pristimantis, with around 400 species ing lineages after speciation, and are therefore indica- described by the classical morphological approach tors of the divergence of those lineages. Under this based on evident qualitative characters, may increase concept, the species is the only biological category considerably. Many Pristimantis are candidates for a above organism, speciation is the process of lineage speciation pattern particularly suitable to originate splitting, and characters are not expected to differ in cryptic and sibling lineages (Lynch & Duellman, 1997). any predictable extent. Under integrative taxonomy, when naming new species, taxonomists should present different lines of evidence to support the hypothesis INTEGRATIVE TAXONOMY that a population is evolving independently. Thus, Taxonomy provides the way to distinguish and com- integrative taxonomy aims to break the circle of con- municate about living and fossil species. For taxono- sidering some characters better than others. Any kind mists, morphology has been the commonest criterion to of character is equally good. And any kind of character delineate and identify those species and, even today, may be useful to propose species taxa hypotheses. By most species descriptions are morphological. The incor- bringing together additional sorts of evidence, empiri- poration of non-morphological suits of characters into cal analyses would allow us to reinforce, reject or taxonomy has been criticized, sometimes by taxono- reconcile hypotheses, making taxonomy a more reli- mists and sometimes by other users of species. For able and scientific activity. Species taxa supported by example, molecular phylogenetics contributed to a several independent and coincident kinds of characters boost of new species that some applied biologists could be considered stable hypotheses. Integrative consider ‘taxonomic inflation’ rather than a real taxonomy thus becomes a new conceptual framework increase in species numbers (Isaac, Mallet & Mace, in which species are hypotheses, and in which inde- 2004). On the other side, molecular biologists who pendent suites of characters are used to construct proposed new ways to identify species based stable species taxa hypotheses. on the comparison of short gene fragments (DNA The practical application of this theoretical basis is barcoding or DNA taxonomy) received much criticism exemplified in this study, where the integration of from a great part of the taxonomic community several independent lines of evidence (morphology, (for a recent review see Vogler & Monaghan, 2006). advertisement calls and phylogenetic analyses of During this debate, a proposal arguing for the com- partial 16S rDNA sequences) allows the description bined use of different suits of characters for species of two new cryptic species of Pristimantis and the descriptions arose from the taxonomic community. solution of some old taxonomic problems. This has been termed integrative taxonomy (Dayrat, 2005). TAXONOMIC BACKGROUND Several phylogenetic methods using combined evi- dence have been proposed to delineate species bound- This study centres on several species of Bolivian and aries (Sites & Marshall, 2004). However, differences in Peruvian frogs of the genus Pristimantis. These the results obtained by different methods or different species were formerly assigned to the genus Eleuth- suites of characters (Wiens & Penkrot, 2002) hamper erodactylus, which was subdivided into several species the incorporation of such methods into practice. This is groups, species series and subgenera by Lynch & one of the main sources of criticism against taxonomic Duellman (1997). Frost et al. (2006) partitioned practices, because uncertainty may lead to arbitrary Eleutherodactylus into several genera that were for- decisions for species descriptions. As recognized by merly considered subgenera (Eleutherodactylus, Crau- integrative taxonomists (Dayrat, 2005), the solution gastor, Syrrophus and Euhyas). However, their might lie in considering species as hypotheses. The analyses did not support the monophyly of Eleuthero- conceptualization of species taxa as hypotheses is dactylus. A more recent phylogenetic analysis with grounded in a general concept of species that consider broader taxon sampling has proposed new taxonomic a species to be a lineage of populations (or metapopu- rearrangements (Hedges, Duellman & Heinicke, lations) diverging separately from all other such lin- 2008). The genus Eleutherodactylus was now eages (De Queiroz, 2005a, b, c). The species, thus restricted to a clade comprising Central American and conceived, becomes a category of biological organiza- Antillean species, Craugastor was restricted to a tion instead of a rank, and the only necessary and middle American clade, and Pristimantis was resur- sufficient property of a species is that it represents a rected for the clade including South American species separately evolving fragment of a metapopulation formerly included in the subgenus Eleutherodactylus. lineage. Properties considered necessary by former We follow the latter authors for the supraspecific species concepts (monophyly, diagnosability, potential taxonomy and therefore all species mentioned in our © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 155, 97–122 CRYPTIC
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