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Bacterial Endosymbiont Infections in Living Fossils

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Bacterial Endosymbiont Infections in Living Fossils Molecular Ecology Resources (2014) doi: 10.1111/1755-0998.12220 Bacterial endosymbiont infections in ‘living fossils’: a case study of North American vaejovid scorpions ROBERT W. BRYSON JR Department of Biology & Burke Museum of Natural History and Culture, University of Washington, Box 351800 Seattle, WA 98195-1800, USA Abstract Bacterial endosymbionts are common among arthropods, and maternally inherited forms can affect the reproductive and behavioural traits of their arthropod hosts. The prevalence of bacterial endosymbionts and their role in scorpion evolution have rarely been investigated. In this study, 61 samples from 40 species of scorpion in the family Vaejovi- dae were screened for the presence of the bacterial endosymbionts Cardinium, Rickettsia, Spiroplasma and Wolbachia. No samples were infected by these bacteria. However, one primer pair specifically designed to amplify Rickettsia amplified nontarget genes of other taxa. Similar off-target amplification using another endosymbiont-specific primer was also found during preliminary screenings. Results caution against the overreliance on previously published screening primers to detect bacterial endosymbionts in host taxa and suggest that primer specificity may be higher in primers targeting nuclear rather than mitochondrial genes. Keywords: Cardinium, DNA barcoding, mitochondrial DNA, Rickettsia, scorpion, Spiroplasma, Vaejovidae, Wolbachia Received 6 September 2012; revision received 2 December 2013; accepted 8 December 2013 mission. In the light of these interactions, endosymbionts Introduction are now regarded as major drivers of arthropod ecology Maternally inherited bacterial endosymbionts are com- and evolution (Engelstadter & Hurst 2009; Fellous et al. mon among arachnids. In spiders, for example, around 2011; Jiggins & Hurst 2011). 20% of all species may be infected by the endosymbiont The prevalence of bacterial endosymbionts and their Cardinium (Duron et al. 2008; Perlman et al. 2010; Stefa- role in scorpion evolution have rarely been investigated. nini & Duron 2012). This bacterium has also been docu- To date, three studies have documented Wolbachia infec- mented at a high frequency in Acari, Opiliones and tions in three families of scorpions (Buthidae, Suesdek- Scorpiones (Martin & Goodacre 2009). Four frequently Rocha et al. 2006; Scorpionidae, Baldo et al. 2007; and studied bacterial endosymbionts have been found in Hemiscorpiidae, Baradaran et al. 2011). The presence of arachnids, including Cardinium, Rickettsia, Spiroplasma Cardinium in scorpions has been documented once and Wolbachia (Goodacre et al. 2006; Martin & Goodacre (Hemiscorpiidae, Martin & Goodacre 2009). In this 2009). study, a diverse sampling of species in the speciose Maternally inherited bacterial endosymbionts are North American scorpion family Vaejovidae was known to affect reproductive and behavioural traits of screened for the presence of Cardinium, Rickettsia, Spiropl- their arthropod hosts (Engelstadter & Hurst 2009). The asma and Wolbachia, four bacterial endosymbionts com- effects of many of these endosymbionts such as Wolbachia monly reported in arachnids. DNA was extracted from or Cardinium can include skewing the sex ratio towards three types of scorpion tissues and, for several species, females (through male killing, feminization and parthe- from multiple individuals. A total of 61 samples were nogenesis) and cytoplasmic incompatibility, both of screened using previously published primers specifically which result in differential reproductive success of designed to amplify genes in targeted bacterial endos- infected versus noninfected females. These mechanisms ymbionts. Although not intended to be an exhaustive are strong selective pressures on bacterial endos- study, results caution against the overreliance on previ- ymbionts which are reliant upon vertical transmission ously published screening primers to detect bacterial through maternal lineages to increase their own trans- endosymbionts in host taxa and suggest that primer specificity may be higher in primers targeting nuclear Correspondence: Robert W. Bryson Jr, Fax: 206-685-3039; E-mail: [email protected] rather than mitochondrial genes. © 2013 John Wiley & Sons Ltd 2 R. W. BRYSON Materials and methods somatic tissues (Dobson et al. 1999; Martin & Goodacre 2009), and infection rates may be low within populations Forty species of scorpion representing seven of the 10 (Jiggins et al. 2001; Duron et al. 2008; Zug & Hammer- genera within the family Vaejovidae (following Prendini stein 2012). Therefore, DNA was also extracted from the & Wheeler 2005) were screened (Table 1). Genomic DNA gonads and surrounding tissues of 15 additional speci- was extracted from leg tissues of 39 specimens using the mens, from seven whole first- or second-stage instars QIAGEN DNeasy Blood and Tissue Kit (Qiagen) follow- and from multiple individuals of eight species (Table 1). ing manufacturer’s recommendations. Maternally inher- In total, 61 samples were screened. ited bacterial endosymbionts may be absent from Table 1 Vaejovid scorpions screened for the bacterial endosymbionts Cardinium, Rickettsia, Spiroplasma and Wolbachia. Taxonomy fol- lows Prendini & Wheeler (2005) Species Locality Tissue type (n) Paruroctonus arenicola USA: California: San Bernardino Co. Leg (1) Paruroctonus becki USA: Arizona: Mohave Co. Leg (1) Paruroctonus boreus USA: Nevada: Elko Co. Leg (1) Paruroctonus gracilior USA: Arizona: Cochise Co. Leg (1) Paruroctonus luteolus USA: California: Inyo Co. Leg (1) Paruroctonus pecos USA: New Mexico: Quay Co. Leg (1) Paruroctonus shulovi USA: Nevada: Clark Co. Leg (1) Paruroctonus silvestrii USA: California: Riverside Co. Leg (1) Paruroctonus utahensis USA: New Mexico: Sante Fe Co. Leg (1) Paruroctonus variabilis USA: California: Fresno Co. Leg (1) Paruroctonus xanthus USA: Arizona: Yuma Co. Leg (1) Pseudouroctonus apacheanus USA: Arizona: Cochise Co. Leg (1) P. apacheanus USA: Arizona: Graham Co. Instar (2) Pseudouroctonus reddelli USA: Texas: Edwards Co. Leg (1) P. reddelli USA: Texas: Bexar Co. Instar (2) Pseudouroctonus williamsi USA: California: San Diego Co. Leg (1) Serradigitus allredi USA: Arizona: Pinal Co. Leg (1) Serradigitus gertschi USA: California: Fresno Co. Leg (1) Serradigitus joshuaensis USA: Arizona: Mohave Co. Leg (1) Serradigitus miscionei USA: Arizona: Pima Co. Leg (1) Serradigitus subtilimanus USA: Arizona: Mohave Co. Leg (1) Serradigitus wupatkiensis USA: Nevada: Clark Co. Leg (1) Smeringurus mesaensis USA: Arizona: Mohave Co. Leg (1) Smeringurus vachoni USA: California: Inyo Co. Leg (1) S. vachoni USA: Nevada: Clark Co. Gonad (2) Uroctonites huachuca USA: Arizona: Santa Cruz Co. Instar (1) U. huachuca USA: Arizona: Cochise Co. Instar (1) Uroctonus franckei USA: California: Inyo Co. Leg (1) Uroctonus mordax USA: California: Marin Co. Leg (1) Vaejovis carolinianus USA: Georgia Leg (1), gonad (4) Vaejovis cashi USA: New Mexico: Hidalgo Co. Leg (1) V. cashi USA: Arizona: Cochise Co. Gonad (5) Vaejovis chisos USA: Texas: Brewster Co. Leg (1), gonad (4) Vaejovis confusus USA: Nevada: Clark Co. Leg (1) Vaejovis feti USA: Arizona: Socorro Co. Leg (1) Vaejovis franckei Mexico: Oaxaca: Cerro Corral del Piedra Leg (1) Vaejovis granulatus Mexico: Morelos: Zempoala Leg (1) Vaejovis hirsuticauda USA: Nevada: Clark Co. Leg (1) Vaejovis intermedius USA: Texas: Val Verde Co. Leg (1) Vaejovis lapidicola USA: Arizona: Coconino Co. Leg (1), instar (1) Vaejovis mumai USA: Arizona: Mohave Co. Leg (1) Vaejovis punctatus Mexico: Aguascalientes: Sierra Fria Leg (1) Vaejovis spinigerus USA: New Mexico: Hidalgo Co. Leg (1) Vaejovis tesselatus Mexico: San Luis Potosı: Alvarez Leg (1) Vaejovis waueri USA: Texas: Terrell Co. Leg (1) © 2013 John Wiley & Sons Ltd BACTERIAL ENDOSYMBIONTS IN SCORPIONS 3 Previously published primers specifically designed to Results amplify genes in targeted bacterial endosymbionts were used in PCRs. For Wolbachia screening, the Wolbachia-spe- No amplicons were produced using the Wolbachia, Cardi- cific primer pair Wspecf/Wspecr (16S-2; Simoes~ et al. nium or Spiroplasma primers. PCRs using the Rickettsia 2011) targeting the 16S rRNA gene was used. This primer primers produced single bands of the expected target detected infections by eight of nine known Wolbachia size in eight samples: Paruroctonus silvestrii (leg tissue), supergroups (Simoes~ et al. 2011), including the super- Paruroctonus utahensis (leg tissue), Serradigitus joshuaensis groups A, B and F previously detected in scorpions (leg tissue), Vaejovis chisos (gonads), Vaejovis feti (leg tis- (Baldo et al. 2007; Baradaran et al. 2011). To screen sam- sue), Vaejovis hirsuticauda (leg tissue), Vaejovis intermedius ples for Cardinium, the primers Car-sp-F/Car-2p-R (leg tissue) and Vaejovis lapidicola (instar). Readable (Nakamura et al. 2009) targeting the 16S rRNA gene and sequence data was obtained for four of these samples gyrF/gyrR (Stefanini & Duron 2012) targeting the gyrase (S. joshuaensis, V. chisos, V. feti and V. hirsuticauda; subunit B gene were used. These primer pairs previously Appendix S1, Supporting information). BLAST results amplified Cardinium in a diverse range of other arach- revealed that these four sequences did not match the tar- nids (Nakamura et al. 2009; Stefanini & Duron 2012). For get taxa. In fact, only one sequence matched any pub- Rickettsia and Spiroplasma PCR screenings, the primer lished gene sequence in the GenBank database (the pair RICS741F/RCIT1197R, designed to amplify the cit- sequence from V. hirsuticauda was
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