Multiple Independent Colonization of the Canary Islands by the Winged
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Molecular Phylogenetics and Evolution 81 (2014) 174–181 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Multiple independent colonization of the Canary Islands by the winged grasshopper genus Sphingonotus Fieber, 1852 ⇑ Martin Husemann a,b, Jana Deppermann c, Axel Hochkirch d, a Department of General Zoology, Institute of Biology/Zoology, University of Halle, D-06120 Halle, Germany b Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, Technische Universität München, D-85350 Freising-Weihenstephan, Germany c University of Oldenburg, Department of Animal Biodiversity and Evolutionary Biology, D-26111 Oldenburg, Germany d Trier University, Department of Biogeography, D-54286 Trier, Germany article info abstract Article history: Volcanic archipelagos represent ideal systems to study processes of colonization, differentiation and Received 3 April 2014 speciation. The Canary Islands are one of the best studied archipelagos, being composed of seven main Revised 12 September 2014 islands with a well-known geological history. Most taxa have colonized these islands stepwise from Accepted 17 September 2014 the African or Iberian mainland from east to west, following their geological origin as well as the predom- Available online 23 September 2014 inating wind direction and ocean currents. Furthermore, within-island radiations have been reported for several taxa. The grasshopper genus Sphingonotus is species-rich and occurs with nine fully winged Keywords: species on the Canary Islands, seven of which are endemic to single or few islands. We inferred a Speciation phylogeny of these species and their North African and Iberian relatives based upon sequences of three Differentiation Island colonization mitochondrial genes and one nuclear gene of 136 specimens. Surprisingly, our results suggest that almost Radiation all Sphingonotus species colonized the archipelago independently from the mainland and nearly no inter- Island biogeography island colonization occurred. Despite their strong flight capabilities, only one pair of endemic species are closely related (S. sublaevis from Gran Canary and S. pachecoi from Lanzarote). Moreover, no within-island speciation events were detected. We hypothesize that passive wind dispersal from the African mainland was the main driver of the colonization process and that most Sphingonotus species are not able to cover inter-island distances by active flight. This, together with strong intrageneric niche overlap might explain the lack of within-island speciation in this taxon. Ó 2014 Elsevier Inc. All rights reserved. 1. Introduction the origin and history of islands is crucial to understand the evolu- tion of island radiations. Oceanic archipelagos represent ideal settings to study coloniza- The Canary Islands are one of the best studied volcanic archipel- tion and differentiation processes (MacArthur and Wilson, 1967; agos, concerning both their geological history (e.g. Ancochea et al., Gilbert, 1980; Emerson, 2002; Whittaker et al., 2008). As such 1990; Acosta et al., 2003) and phylogeography (reviewed in Juan the Galapagos, the Caribbean, Hawaii and the Canary Islands have et al., 2000). Due to their geographic position, the African mainland become model systems for biogeographic and evolutionary is the predominating colonization source (Juan et al., 2000). Many research (Gillespie et al., 1994a; Emerson et al., 1999, 2000a; taxa have undergone radiations within the archipelago subsequent Grant and Grant, 2002; Shaw, 2002; Losos, 2009). The main pro- to a single colonization event. Most of these radiations follow a cesses determining speciation on islands are colonization, extinc- simple stepping stone model from east to west following the pre- tion and speciation as a result of geographical barriers or vailing ocean currents and wind directions (e.g. Díaz-Pérez et al., ecological niche differentiation (MacArthur and Wilson, 1967; 2008; Hochkirch and Görzig, 2009). However, multiple variants Emerson, 2008; Losos, 2009). The geographical setting and the geo- of this pattern have been found, including back-colonization, logical history of an archipelago have strong effects on the relative within-island speciation or reverse colonization from the Canary importance of each of these processes. Hence, a good knowledge on Islands to the African mainland (Juan et al., 2000). In many cases, the successful colonization of one island is followed by subsequent radiation on the complete archipelago. This has been reported for ⇑ Corresponding author. Fax: +49 651 201 3851. darkling beetles of the genus Pimelia (Contreras-Díaz et al., 2003) E-mail address: [email protected] (A. Hochkirch). and Hegeter (Juan et al., 1996), ground beetles of the genus Calathus http://dx.doi.org/10.1016/j.ympev.2014.09.017 1055-7903/Ó 2014 Elsevier Inc. All rights reserved. M. Husemann et al. / Molecular Phylogenetics and Evolution 81 (2014) 174–181 175 (Emerson et al., 2000a), bark beetles of the genus Tarphius intra- and inter-island colonization history with a strong influence (Emerson et al., 2000b), Gallotia lizards (Cox et al., 2010), Chalcides of the prevailing wind direction and ocean currents and the geolog- skinks (Brown and Pestano, 1998), and plants of the genus Echium ical history of the islands. (Böhle et al., 1996). However, the individual patterns and timing of colonization differ depending on the taxon and its intrinsic charac- 2. Methods teristics (Juan et al., 2000). Orthoptera represent interesting model systems for the study of 2.1. DNA sequencing island biogeography as they include both mobile as well as rather sessile taxa, which allows a comparison of the colonization mech- A total of 136 specimens of Canarian, NW African and European anisms in organisms with different mobility. The phylogenies of Sphingonotus species as well as some other Oedipodinae have been several Canarian Orthoptera have already been reconstructed collected from 2002 to 2012 (Table S1). The specimens were stored (López et al., 2007; Arnedo et al., 2008; Hochkirch and Görzig, either in 99% ethanol p.a. or frozen. We chose the Schistocerca gre- 2009). However, most of these taxa have rather limited dispersal garia Forskål, 1775, Oedipoda caerulescens (Linnaeus, 1758), Vossel- abilities. For example, a phylogenetic study of the flightless genus eriana arabica (Mishchenko, 1937), Helioscirtus capsitanus (Bonnet, Arminda has revealed a stepwise colonization pattern which has 1884) and three species of the genus Thalpomena (T. coerulescens led to single island endemics (Hochkirch and Görzig, 2009). Simi- (Uvarov, 1923), T. rungsi (Dirsh, 1949), T. algeriana (Lucas, 1849)) larly, the very sedentary genus complex Acrostira/Purpuraria con- and Sphingoderus carinatus (Saussure, 1888) as outgroups. These sists mainly of single island endemics, albeit with very close taxa represent different divergence levels to Sphingonotus as has genetic relationships (López et al., 2007). In the katydid genus Cal- been demonstrated in previous studies (Fries et al., 2007; Chapco liphona, which has variable wing lengths, phylogenetic analyses and Contreras, 2011; Husemann et al., 2012, 2013b). The DNeasy suggested an inter-island taxon cycling process (Arnedo et al., Blood and Tissue Kit (Qiagen, Hilden, Germany) was used for 2008). DNA extraction from femoral or thoracic muscle tissue following Here, we analyze the island biogeography of a grasshopper the manufacturer’s protocol. Four gene fragments (three mitochon- genus with strong flight abilities, which nevertheless has a high drial, one nuclear) were amplified: (1) NADH dehydrogenase sub- number of endemic species on the Canary Islands. The genus unit 5 (ND5, 1050 bp), (2) 12s rRNA (12s, 350 bp), (3) a fragment Sphingonotus Fieber, 1852 is one of the most species-rich grasshop- containing parts of 16s rRNA, tRNA-Leu and NADH dehydrogenase per genera worldwide, with currently 145 described species in subunit 1 (NDS, 537 bp), (4) internal transcribed spacer 2 (ITS2, three subgenera (Neosphingonotus 14 species, Parasphingonotus 3 308 bp). Primer information is given in Table 1. PCR conditions species, Sphingonotus s. s. 128 species) (Eades et al., 2014). Nine are provided elsewhere (Husemann et al., 2012; Husemann et al., Sphingonotus species occur on the Canary Islands, seven of which 2013a,b). The 5Prime HotMasterMix (5Prime, Hilden, Germany) are endemic to single or two islands: (1) S. pachecoi (Bolívar, and the HotStarTaq Master Mix Kit (Qiagen) were used for ampli- 1908) from Lanzarote; (2) S. fuerteventurae Husemann, 2008 from fication. The PCR product was purified using either the Qiaex II Gel Fuerteventura; (3) S. rugosus (Bland, 1998) from Lanzarote and Extraction Kit (Qiagen) or the Roche PCR product purification kit Fuerteventura; (4) S. sublaevis (Bolívar, 1908) from Gran Canaria; (Roche, Risch, Switzerland) according to the manufacturer’s proto- (5) S. guanchus (Johnsen, 1985) from Gran Canaria; (6) S. picteti cols. Sequencing was performed with the Big Dye sequencing kit (Krauss, 1892) from coastal Tenerife; and (7) S. willemsei Mists- (Perkin Elmer, Cheshire, UK) for sequencing reactions on a Per- henko, 1937 from subalpine Tenerife (Cañadas). Two further spe- kin–Elmer ABI automated sequencer or with the DYEnamic ET Ter- cies, S. savignyi (Saussure 1884) and S. rubescens (Walker, 1870) minator Cycle Sequencing Premixkit (GE Healthcare, Munich, are widely distributed from north-western