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Molecular and Morphometric Data Indicate a New Species of the Aphid Genus Rhopalosiphum (Hemiptera: Aphididae) Author(S): I

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Molecular and Morphometric Data Indicate a New Species of the Aphid Genus Rhopalosiphum (Hemiptera: Aphididae) Author(S): I Molecular and Morphometric Data Indicate a New Species of the Aphid Genus Rhopalosiphum (Hemiptera: Aphididae) Author(s): I. Valenzuela, V. F. Eastop, P. M. Ridland, and A. R. Weeks Source: Annals of the Entomological Society of America, 102(6):914-924. 2009. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1603/008.102.0602 URL: http://www.bioone.org/doi/full/10.1603/008.102.0602 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. SYSTEMATICS Molecular and Morphometric Data Indicate a New Species of the Aphid Genus Rhopalosiphum (Hemiptera: Aphididae) 1,2,3 4 2 1 I. VALENZUELA, V. F. EASTOP, P. M. RIDLAND, AND A. R. WEEKS Ann. Entomol. Soc. Am. 102(6): 914Ð924 (2009) ABSTRACT Here, we provide evidence for a new aphid species from the genus Rhopalosiphum Koch, based upon an Australian survey of variation in the mitochondrial cytochrome oxidase I gene, and subsequently validated by cytochrome b, nuclear microsatellites, nuclear sequence characterized ampliÞed region locus, and karyotypic analyses. Despite the new species being morphologically very similar to Rhopalosiphum padi (L.), there was signiÞcant genetic differentiation, with the new species being closer to the Rhopalosiphum insertum (Walker) group. Karyotypic analyses indicated a putative hybrid origin for the new species, but mitochondrial and nuclear DNA sequence data showed that the available Australian and overseas populations of Rhopalosiphum spp. did not serve as parental lineages. Diagnostic methods were developed that enabled the identiÞcation of the new species based on morphometric data and a polymerase chain reaction-restriction fragment length polymorphism based molecular technique. KEY WORDS hybridization, cryptic, karyotype, mitochondrial DNA, nuclear DNA Surveys of molecular variation in nuclear and mito- conditions, molecular techniques, such as karyotype chondrial DNA sequences of invertebrates are in- and DNA studies, have proven more efÞcient in sep- creasingly being used to identify cryptic species even arating morphologically indistinguishable taxa. For ex- in well-studied genera. Examples include the recent ample, two studies on the genetic diversity of Rhopa- discovery of a new species of Drosophila based on losiphum revealed previously unrecorded and microsatellite sequence data (Schiffer et al. 2004), the undescribed cryptic taxa. In Australia, Hales and Co- detection of new taxa of Neotropical skipper butter- wen (1990) characterized allozyme patterns and chro- ßies (Hebert et al. 2004), the molecular characteriza- mosome numbers of Rhopalosiphum maidis (Fitch), tion of two cryptic species of bumblebees (Ellis et al. Rhopalosiphum padi (L.), Rhopalosiphum rufiabdomi- 2005), and the discovery of various cryptic parasitoid nale (Sasaki), and Rhopalosiphum near insertum ßies from the genus Belvosia Robineau-Desvoidy (Walker) [see Blackman and Eastop (2006) for R. (Smith et al. 2006). Once new molecular variants are insertum and R. near insertum details] with results established, simple molecular tests also can be devel- conforming to previous overseas records. But, they oped that distinguish between the cryptic taxa. For found a R. padi-like form that had a diploid chromo- example, polymerase chain reaction (PCR)-restric- some number of 2n ϭ 9 (compared with 2n ϭ 8 for the tion fragment length polymorphism (RFLP) analysis other species) and a unique allozyme pattern. They of the mitochondrial genes cytochrome oxidase subunit postulated that this new taxon could be a hybrid be- I (COI) (Carew et al. 2005, 2007) and cytochrome b tween R. padi and R insertum because of morpholog- (Ellis et al. 2006), and the intragenic transcribed ical similarities, but the allozyme patterns did not spacer (ITS) nuclear ribosomal region have been de- support this idea, and the authors suggested the R. veloped recently (Carew et al. 2004). padi-like form was most likely a new undescribed In aphids, groups of closely related taxa can be species. In New Zealand, Bulman et al. (2005) de- particularly difÞcult to identify, mainly because of the tected two undescribed taxa using karyotype, random high plastic nature of aphid morphology and the pres- ampliÞed polymorphic DNA markers, cytochrome b, ence of cryptic species, hybrids, and complex groups and ITS sequence data. Molecular results revealed a R. of species (Blackman et al. 1987a, Blackman and padi-like form that had signiÞcant molecular differ- Spence 1994, Blackman and Eastop 2007). Under these ences from local and overseas populations of R. padi. Analysis of ribosomal RNA sequence data, however, 1 Centre for Environmental Stress and Adaptation Research, The related this taxon (called R. padi T) to the R. insertum University of Melbourne, Parkville, Victoria 3010, Australia. group that included a European taxon and a New 2 Department of Primary Industries, KnoxÞeld Centre, Private Bag Zealand taxon called R. near insertum. The authors 15, Ferntree Gully Delivery Centre, Victoria 3156, Australia. concluded that R. padi T, was an undescribed species 3 Corresponding author, e-mail: [email protected]. 4 Natural History Museum, Cromwell Rd., London SW7 5BD, of Rhopalosiphum. Moreover, the same DNA se- United Kingdom. quence data also found that New Zealand R. near 0013-8746/09/0914Ð0924$04.00/0 ᭧ 2009 Entomological Society of America November 2009 VALENZUELA ET AL.: MOLECULAR CHARACTERIZATION OF AN APHID SPECIES 915 insertum was signiÞcantly different from the European ical studies have been conducted on these taxa that taxon. These studies show how karyotypic and mo- addressed speciÞc questions on their taxonomy and lecular techniques are capable of characterizing new phylogenetic relationships. Thus, our study intended taxonomic entities that were previously unknown be- Þrstly to detect Rhopalosiphum cryptic species that cause of their cryptic morphology and habitat with had previously been recorded by allozymes and karyo- more common and widespread forms. type studies in Australia (Hales and Cowen 1990) and Rhopalosiphum Koch has Ϸ17 species, which are maintain cultures of these in the laboratory so further mainly associated with rosaceous trees as primary molecular and morphological studies could be under- hosts and monocotyledonous plants as secondary taken. We used genetic markers, including karyotype hosts (Remaudie`re and Remaudie`re 1997, Blackman counts, mitochondrial COI, and cytochrome b se- and Eastop 2006). Native species from the northern quencing as well as nuclear microsatellites and a temperate zones of both the New World and the Old nuclear sequence characterized ampliÞed region World have been found; however, the geographic or- (SCAR) marker (Simon et al. 1999) to reveal phylo- igins of some species remain uncertain because of genetic relationships between Australian and overseas the worldwide propagation with agricultural practices populations of R. padi and investigate putative hybrid (Halbert and Voetglin 1998). Taxonomic surveys have origins for cryptic taxa. We searched for new mor- been conducted in Canada and North America (Rich- phological characters that could discriminate between ards, 1960, 1962), Britain (Stroyan 1984), Fennoscandia cryptic species and their close relatives, and con- and Denmark (Heie 1986), the Iberian peninsula (Nieto ducted a canonical discriminant analysis from a range Nafrõ´a et al. 2005), northeastern India (Raychaudhuri of morphometrics in apterous and alate aphids. Addi- 1980), eastern Siberia (Pashchenko 1988), Japan (Taka- tionally, mitochondrial COI sequence data were used hashi 1965, Torikura 1991), and Australia (Eastop 1966), to develop a simple and accurate PCR-RFLPÐbased and more recent molecular studies have addressed ques- diagnostic method for species identiÞcation in the tions regarding levels of genetic diversity found between genus. Rhopalosiphum species (Hales and Cowen 1990, Bulman et al. 2005, Yeh et al. 2005, Valenzuela et al. 2007). Materials and Methods Molecular markers have been decisive in detecting cryptic variation in the genus. For example, Delmotte Aphid Collections. Species from the genus Rhopa- et al. (2003) characterized two mitochondrial cyto- losiphum were collected in 2004Ð2007 in Victoria, chrome b haplotypes of R. padi as two genetically southeastern Australia (Fig. 1), from a range of dif- distinct lineages that diverged 0.4 MYA, an obligate ferent locations and host plants (Table 1). They were asexual lineage of hybrid origin with a mitochondrial individually placed into Solo cups (Highland Park, IL) (mt)DNA haplotype I, and a second group containing containing a barley, Hordeum vulgare L., seedling and sexual and
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