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Hemiptera: Aphididae: Macrosiphini) Living on Ferns in Costa Rica and Mexico

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Hemiptera: Aphididae: Macrosiphini) Living on Ferns in Costa Rica and Mexico 509 A new aphid genus and species (Hemiptera: Aphididae: Macrosiphini) living on ferns in Costa Rica and Mexico Juan M. Nieto Nafrı´a,1 Nicola´sPe´rez Hidalgo, David Martı´nez-Torres, William Villalobos Muller Abstract—Aphid species colonising ferns belong to the subfamily Aphidinae (Hemiptera: Aphididae) and the majority of these to the tribe Macrosiphini. A new genus in this tribe and its type species: Gibbomyzus pteridophytorum new genus, new species, are established. Apterous and alate viviparous females are described from specimens collected on Blechnum buchtienii Rosenstock (Blechnaceae) in Costa Rica and on Pteridium aquilinum (Linnaeus) Kuhn (Dennstaedtiaceae) and an unidentified fern in Mexico. The taxonomic validity of the two new taxa is discussed based on morphological and molecular data. Morphologically, the new genus is compared with genera with swollen siphunculi recorded in the New World, and also with genera living on ferns anywhere in the world. The identification key by Blackman and Eastop to aphids living on ferns is modified. Molecular analyses were carried out on the sequences of a fragment of the mitochondrial gene encoding for cytochrome c oxidase subunit 1 and of a fragment of the nuclear gene encoding elongation factor-1 alpha. In both analyses, G. pteridophytorum new species sequences showed considerable divergence (,4% or more) from those of 23 other species from diverse genera of Macrosiphini, supporting the conclusions of the morphological study and justifying the establishment of the new genus. Re´sume´—Les espe`ces de pucerons qui colonisent des fouge`res appartiennent a` la sous-famille Aphidinae (Hemiptera: Aphididae) et la majorite´ d’entre elles a` la tribu Macrosiphini. Un nouveau genre de cette tribu et son espe`ce typique sont e´tablis : Gibbomyzus pteridophytorum, nouveau genre, nouvelle espe`ce, avec la description des femelles vivipares apte`res et aile´es collecte´es sur Blechnum buchtienii Rosenstock (Blechnaceae) au Costa Rica, et sur Pteridium aquilinum (Linnaeus) Kuhn (Dennstaedtiaceae) et une fouge`re non identifie´e au Mexique. La validite´ taxonomique des deux nouveaux taxons est discute´e morphologiquement par la comparaison du nouveau genre avec des genres cite´s en Ame´rique qui pre´sentent des cornicules gonfle´es, et des genres qui habitent sur des fouge`res dans n’importe quelle partie du monde. Une modification de la cle´ d’identification de Blackman et Eastop pour les pucerons qui habitent sur les fouge`res est pre´sente´e. Des analyses mole´culaires ont e´te´ re´alise´es sur les se´quences d’un fragment du ge`ne mitochondrial qui code pour la sous-unite´1du cytochrome oxydase et d’un fragment du ge`ne nucle´aire qui code pour le facteur d’e´longation 1 alpha. Dans les deux analyses les se´quences de G. pteridophytorum nouvelle espe`ce ont une divergence conside´rable (4% ou plus) avec celles de 23 espe`ces de plusieurs genres de Macrosiphini, en appuyant les conclusions de l’e´tude morphologique, et en justifiant qu’un nouveau genre soit e´tabli. Introduction (N.N., P.H., V.M.) collected several viviparous female aphids on Blechnum buchtienii Rosenstock During expeditions to Costa Rica in 2008, (Blechnaceae) in Cerro Buenavista or Cerro de la M.P. Mier Durante and three of the authors Muerte (Talamanca mountain range). These were Received 27 August 2012. Accepted 3 January 2013. First published online 14 June 2013. J.M. Nieto Nafrı´a,1 N. Pe´rez Hidalgo, Departamento de Biodiversidad y Gestio´n Ambiental, Universidad de Leo´n, 24071 Leon, Spain D. Martı´nez-Torres, Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de Vale`ncia, Apdo. Correos 22085, 46071 Valencia, Spain W. Villalobos Muller, Centro de Investigacio´n en Biologı´a Celular y Molecular, Universidad de Costa Rica, 11501-2060, San Jose´, Costa Rica 1Corresponding author (e-mail: [email protected]). Subject editor: Patrice Bouchard doi:10.4039/tce.2013.32 http://zoobank.org/urn:lsid:zoobank.org:pub:EC5B1AF2-BA7F-4A51-B2D4-B4B4FCFFF1B8 Can. Entomol. 145: 509–520 (2013) ᭧ 2013 Entomological Society of Canada 510 Can. Entomol. Vol. 145, 2013 identified as belonging to the tribe Macrosiphini software (Leica Microsystems Imaging Solutions (Hemiptera: Aphididae: Aphidinae) sensu the Ltd., Cambridge, United Kingdom). ‘‘Remaudie`re, Quednau, and Stroyan extended Molecular phylogenetic analyses were done classification’’ (Nieto Nafrı´a and Favret 2011). based (1) on a fragment of the mitochondrial Given their peculiar characteristics we believe they DNA containing the 50 region of the cytochrome represent a new species. Subsequently, one of the c oxidase 1 (COI) and (2) on a fragment of the authors (V.M.) visited the capture locality several nuclear gene coding for elongation factor-1 alpha times to monitor the population and verifying (EF1a) of three specimens. that the aphids developed and reproduced on the Total DNA was extracted separately from host plant. three specimens. DNA extraction was done fol- Specimens caught on ferns in Mexico lowing the HotSHOT (Hot Sodium HydrOxide belonging to the collection ge´nerale d’aphids of and Tris) method (Truett et al. 2000). Voucher the Muse´um national d’Histoire naturelle, Paris, specimens are the colony mates, presumed to be France were also examined. genetic clones, examined and described below. Polymerase chain reaction (PCR) amplifica- Material and methods tions of the two gene fragments analysed were done using 3 ml of the extracted DNA in 50 ml A comparative morphological study was total reaction volumes. A 710 base pair fragment conducted on species in genera (i) whose apterae of the 50 region of COI was amplified using possess swollen siphunculi and have been primers LCO1490 and HCO2198 described by recorded in North America or (ii) are known to Folmer et al. (1994). PCR conditions for COI feed on ferns. Along with the new material from amplification were as follows: 94 8C for 1 min- Costa Rica, we also examined aphid specimens ute; 35 cycles of 94 8C for 30 seconds, 48 8C for in the collections of the Muse´um national 1 minute and 68 8C for 1 minute; a final exten- d’Histoire naturelle (Paris, France) and the Uni- sion step of 7 minutes at 68 8C was included after versidad de Leo´n (Leon, Spain). We consulted the cycling. Amplification of the EF1a fragment works of Robinson (1966), Miyazaki (1968, 1971), was done using two consecutive PCR reactions Hille Ris Lambers (1969), Ghosh (1974), Ghosh with primers Efs175 (Moran et al. 1999) and Efr1 et al. (1977), Moritsu (1983), Remaudie`re (1983), (50GTGTGGCAATSCAANACNGGAGT30)in Cook (1984), Chakrabarti and Banerjee (1989), the first reaction and then primers Efs175 and Heie (1992, 1994, 1995), Remaudie`re and Mun˜oz Efr2 (50TTGGAAATTTGACCNGGGTGRTT30) Viveros (1992), Foottit and Richards (1993), in the second semi-nested reaction. PCR condi- Remaudie`re and Remaudie`re (1997), Lee et al. tions used in the first reaction were: 94 8Cfor (2002), Sorin and Arakawa (2005), Blackman 1 minute; 40 cycles of 94 8C for 30 seconds, 50 8C and Eastop (2006), and Blackman (2010). for 1 minute and 68 8C for 1.5 minutes; a final The type specimens are preserved in micro- extension step of 7 minutes at 68 8C was included scopic slides with a water-soluble mounting after cycling. The semi-nested PCR was done medium (Nieto Nafrı´a and Mier Durante 1988). similarly but using 52 8C for the annealing step and The specimens for the molecular analysis were using 1 ml of the first PCR product. preserved in 96% ethanol until processing. Data PCR products were purified by ammonium pre- on the capture of the studied specimens can be cipitation and reconstituted in 10 ml of LTE buffer seen in the ‘‘Types’’ section in the description of (10 mM Tris, 0.1 mM EDTA). Direct sequencing the new species. of amplified fragments was done in both directions Measurements of the slide-mounted specimens usingPCRprimers(Efr2wasusedasreversepri- were made according to Nieto Nafrı´a and Mier mer for sequencing the EF1a fragment). Sequen- Durante (1988) with an ocular micrometre. The cing was conducted using the Big Dye Terminator measurements are lengths except when indicated v3.1 Cycle Sequencing Kit (Applied Biosystems, that they are a width or diameter. A camera lucida Forster City, California, United States of America) fittedtothemicroscopewasusedforthedrawings, following the manufacturer’s instructions, and and the photomicrographs were taken with a Leica sampleswereloadedontoanABI3700automated DC digital camera with IM 1000 version 1.10 sequencer (Applied Biosystems). ᭧ 2013 Entomological Society of Canada Nieto Nafrı´a et al. 511 Chromatograms were revised and sequences Cerro de la Muerte (Mirador de los Quetzales, assembled using the Staden package v1.6.0 98380N, 838510W, 2900 m), B. buchtienii, 28-ii- (Bonfield et al. 1995). Multiple alignments were 2008, Nieto Nafrı´a, Mier Durante, Villalobos done with Clustal X v2.1 (Larkin et al. 2007) Muller and Pe´rez Hidalgo leg.; Zoological Col- with gap opening and gap extension penalties of lection of the University of Leo´n (CZULE). 10.0 and 0.2, respectively. Phylogenetic and Paratypes: 14 apterous viviparous females and molecular evolutionary analyses were conducted three alate viviparous females caught at same using MEGA version 5 (Tamura et al. 2011). time as the holotype; CZULE, Leon (Spain), and Museo de Zoologı´a, Universidad de Costa Rica, San Pedro de Montes de Oca (Costa Rica); one Results and discussion apterous viviparous female, MEXICO: Mexico The combined description of these new spe- state, Popocate´petl (3000 m), unidentified fern, cies and new genus is made under Article 13.4 of 1.x.79, G. Remaudie`re leg., register number the International Code of Zoological Nomen- 06174; one apterous viviparous female, MEXICO: clature (International Commission on Zoological Michoacan state, Paricutin (,2500 m), Pteridium Nomenclature 1999).
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