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(Trichoptera: Philopotamidae) Using Molecular Methods

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(Trichoptera: Philopotamidae) Using Molecular Methods Molecular Phylogenetics and Evolution 79 (2014) 433–442 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev The age, ancestral distribution and radiation of Chimarra (Trichoptera: Philopotamidae) using molecular methods ⇑ Emma Wahlberg a,b, , Kjell Arne Johanson b a Department of Zoology, University of Stockholm, 10691 Stockholm, Sweden b Department of Zoology, Swedish Museum of Natural History, Box 50007, 10405 Stockholm, Sweden article info abstract Article history: The phylogeny of Chimarra has previously been examined using morphological characters for a smaller Received 6 March 2014 subset of taxa and geographical representativeness. Here molecular data from three genes (COI, CAD Revised 11 June 2014 and POL-II) are used to reconstruct the phylogeny of the genus. The results show Chimarra to be mono- Accepted 26 June 2014 phyletic, and that some of the sister groups are paraphyletic. Previous hypotheses regarding the relation- Available online 5 July 2014 ships of subgenera within the genus are corroborated but incongruences are also found compared to morphological characters that have been used in keys. The origin of the genus is explored using three dif- Keywords: ferent hypotheses of biogeographical region. The biogeography analyses reveal an origin in the Neotrop- Caddisflies ical region and a subsequent rapid radiation, with dispersal into the Oriental, Palaearctic and Australasian Taxonomy Biogeography regions and secondarily to the Nearctic region. The Afrotropical region has been colonized in several inde- Zoogeography pendent events. The molecular dating using a relaxed clock and calibration with four fossil species indi- Phylogeny cates that Chimarra is about 138 million years old, and that the radiation out of the Neotropical region occurred approximately 124 million years ago. Ó 2014 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). 1. Introduction The Philopotamidae Stephens, 1829 are divided into three sub- families; one of them being Chimarrinae Rambur, 1842, to which The higher classification of Trichoptera Kirby, 1813 has been the genera Chimarra Stephens, 1829, Chimarrhodella Lestage, repeatedly reconfigured and re-evaluated through analyses of both 1925 and Edidiehlia Malicky, 1993 belong. With almost 700 morphological and molecular data (e.g. Frania and Wiggins, 1997; described species, Chimarra is the second largest genus in Trichop- Kjer et al., 2001, 2002; Holzenthal et al., 2007; Johanson and Malm, tera after Rhyacophila Pictet, 1834 (Rhyacophilidae Stephens, 1836) 2010; Malm et al., 2013). Analyses of molecular data have made it (Johanson and Oláh, 2012). The number of species described from possible to reinterpret our understanding of the evolutionary his- the world’s major biogeographic regions (sensu Wallace, 1876) tory of the order, and also to confirm previous theories. Molecular reflects a high diversity concentrated in the tropics, with 229 spe- data apparently increases the resolution, especially at family and cies described from the Neotropical region, 321 from the Oriental, genus level (Malm and Johanson, 2011; Johanson et al., 2012). 105 from the Australasian, 83 from the Afrotropical, 39 from the There are presently over 14,000 described species in the order Nearctic and 3 species from the western part of the Palearctic (Morse, 2013), and though the diversity of the order does not reach region. This is somewhat consistent with the Trichoptera order in the massive numbers of the orders Coleoptera, Diptera and Hyme- general, where the largest diversity is found in the humid tropics noptera caddisflies are important in biodiversity and environmen- (de Moor and Ivanov, 2008). Blahnik (2005) outlines the general tal research. As the larvae of Trichoptera are sensitive to pollution, taxonomy of Philopotamidae, including Chimarra and its putative sedimentation and other impacts on freshwater systems from nat- sister taxa, and points out that it is presently unclear how these ural and anthropogenic causes, they have been regarded as valu- genera are related. As with Philopotamidae, Chimarra has been able indicators on ecological and environmental status subject to taxonomic re-positioning, with the addition and removal (Einheuser et al., 2012; Ratia et al., 2012; Ruiz-Garcia et al., 2012). of taxa (Blahnik, 1997). The number of described species increases constantly and the amount of available taxa today opens up for comprehensive analyses of the phylogenetic history of the group. ⇑ Corresponding author at: Department of Zoology, Stockholm University, SE- 10691 Stockholm, Sweden. The larva of Philopotamidae construct nests as a long, sock-like E-mail addresses: [email protected] (E. Wahlberg), kjell.arne. tube of silk and the labrum shape is unique to the order [email protected] (K.A. Johanson). (Holzenthal et al., 2007). The nests of the larvae are fixed, as in http://dx.doi.org/10.1016/j.ympev.2014.06.023 1055-7903/Ó 2014 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). 434 E. Wahlberg, K.A. Johanson / Molecular Phylogenetics and Evolution 79 (2014) 433–442 all representatives of the suborder Annulipalpia. The larva of that the Eurasian species are descendants of the Afrotropical Chimarra is recognized by the presence of a deep and asymmetrical lineage rather than North American ones. Both Ross and Blahnik clypeal notch (Ross, 1944). The adults range from black and dark base their theories on the similarity of Asian and North American brown to yellow and dark red in color. The average body length species, and according to both authors the Neotropical region is typically 3–8 mm including wings. The general diagnosis of adult would include of both early species and ones more closely related Chimarra is the presence of a spur formula 1, 4, 4; and the anal vein to the Asian fauna, but they reach very different conclusions 2 of the hind wings is fused with the anal vein 1 forming a closed regarding the major lineages and their dispersal. Due to the lack cell (Blahnik, 1998). Four subgenera are recognized in Chimarra; of well-founded fossil records and close morphological resem- Chimarrita Blahnik, 1997, Curgia Walker, 1860, Otarrha Blahnik, blance of extant species, we aim at resolving the phylogenetic his- 2002, and Chimarra Stephens, 1829. The subgenus Chimarra occurs tory of the genus by using molecular dating methods. We use in most parts of the world, except Antarctica, while the three other different biogeographical divisions to resolve patterns of origin, subgenera are confined to the Neotropical region (Johanson and dispersal and vicariance events as well as outlining a hypothesis Oláh, 2012). The subgenera within Chimarra are not distinctive of the phylogenetic relationships of Chimarra and its subgenera. morphologically but Blahnik (1998) provides an outline of the morphology of subgenera together with a key. However, the char- 2. Material and methods acters distinguishing the subgenus Chimarra are ambiguous; the curved stem of the radial sector (Rs) (Supplementary Fig. 1a)is 2.1. Taxon sampling not present in several Afrotropical species, and morphological dif- ferences in the genitalia are vaguely defined and are often a com- In order to better understand the relationship between Chimarra bination of characters. The subgenus Otarrha share many and closely related genera, representatives from the genera characters with some species in the subgenera Chimarra and Dolophilodes Ulmer, 1909 (including the subgenera Dolophilodes Chimarrita, but clearly separated from those by the presence of a Ulmer, 1909, Hydrobiosella Tillyard, 1926 and Sortosa Navás, mesal division of tergum X in males and ventral process of segment 1918), Wormaldia McLachlan, 1865, Philopotamus Stephens, 1829, VII in females. The subgenera Chimarrita and Curgia are distinctive Gunungiella Ulmer, 1913 and Chimarrhodella were included in the only by a combination of more or less inconspicuous genital char- analysis as ingroups. Taxa from the families Stenopsychidae acters. The biogeographical patterns are apparently the clearest Martynov, 1924, Hydroptilidae Stephens, 1836, Hydropsychidae distinction of the subgenera, except for the cosmopolitan subgenus Curtis, 1835 and Rhyacophilidae were included as an outgroup. Chimarra. In their recent work on Chimarra in Vietnam, Blahnik Specimens were sampled from a variety of localities with wide, et al. (2012) pointed out the differences in the configuration of almost cosmopolitan coverage. The Chimarra species have been the anal veins of the front wings among species (Supplementary identified to subgenera based on Blahnik (1998). Out of 117 taxa Fig. 1), indicating that these could maybe be used in revealing in the ingroup, 94 are Chimarra and 110 Philopotamidae. The the phylogenetic history of the genus. complete taxon set and citation is listed in Supplementary data 1. Sampling of material was carried out by staff and associates of 1.1. The biogeography of Chimarra the Swedish Museum of Natural History (NHRS). Both Blahnik (1998) and Ross (1956) suggested that the ances- tral area of diversification was South America, preceding the 2.2. DNA amplification and sequencing breakup of Gondwana. There are few known fossils of Chimarra, which is problematic when trying to infer the time and area of ori-
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