Winnie Hallwachs

University of Guelph, Guelph, Ontario, Canada

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Publications (24)103.84 Total impact

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    Dataset: Janzen eyes mimicrySI 2010
    Daniel H Janzen, Winnie Hallwachs, John M Burns
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    Dataset: Smith MA et al 2012 s001
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    Dataset: Smith MA et al 2012 s002
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    Dataset: Smith MA et al 2012 s003
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    Article: Wolbachia and DNA Barcoding Insects: Patterns, Potential, and Problems
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    ABSTRACT: Wolbachia is a genus of bacterial endosymbionts that impacts the breeding systems of their hosts. Wolbachia can confuse the patterns of mitochondrial variation, including DNA barcodes, because it influences the pathways through which mitochondria are inherited. We examined the extent to which these endosymbionts are detected in routine DNA barcoding, assessed their impact upon the insect sequence divergence and identification accuracy, and considered the variation present in Wolbachia COI. Using both standard PCR assays (Wolbachia surface coding protein – wsp), and bacterial COI fragments we found evidence of Wolbachia in insect total genomic extracts created for DNA barcoding library construction. When .2 million insect COI trace files were examined on the Barcode of Life Datasystem (BOLD) Wolbachia COI was present in 0.16% of the cases. It is possible to generate Wolbachia COI using standard insect primers; however, that amplicon was never confused with the COI of the host. Wolbachia alleles recovered were predominantly Supergroup A and were broadly distributed geographically and phylogenetically. We conclude that the presence of the Wolbachia DNA in total genomic extracts made from insects is unlikely to compromise the accuracy of the DNA barcode library; in fact, the ability to query this DNA library (the database and the extracts) for endosymbionts is one of the ancillary benefits of such a large scale endeavor – for which we provide several examples. It is our conclusion that regular assays for Wolbachia presence and type can, and should, be adopted by large scale insect barcoding initiatives. While COI is one of the five multi-locus sequence typing (MLST) genes used for categorizing Wolbachia, there is limited overlap with the eukaryotic DNA barcode region.
    PLoS ONE 05/2012; 7(5):e36514. doi:10.1371/journal.pone.0036514. · 4.09 Impact Factor
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    Article: Utility of the DNA barcoding gene fragment for parasitic wasp phylogeny (Hymenoptera: Ichneumonoidea): data release and new measure of taxonomic congruence.
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    ABSTRACT: The enormous cytochrome oxidase subunit I (COI) sequence database being assembled from the various DNA barcoding projects as well as from independent phylogenetic studies constitutes an almost unprecedented amount of data for molecular systematics, in addition to its role in species identification and discovery. As part of a study of the potential of this gene fragment to improve the accuracy of phylogenetic reconstructions, and in particular, exploring the effects of dense taxon sampling, we have assembled a data set for the hyperdiverse, cosmopolitan parasitic wasp superfamily Ichneumonoidea, including the release of 1793 unpublished sequences. Of approximately 84 currently recognized Ichneumonoidea subfamilies, 2500 genera and 41,000 described species, barcoding 5'-COI data were assembled for 4168 putative species-level terminals (many undescribed), representing 671 genera and all but ten of the currently recognized subfamilies. After the removal of identical and near-identical sequences, the 4174 initial sequences were reduced to 3278. We show that when subjected to phylogenetic analysis using both maximum likelihood and parsimony, there is a broad correlation between taxonomic congruence and number of included sequences. We additionally present a new measure of taxonomic congruence based upon the Simpson diversity index, the Simpson dominance index, which gives greater weight to morphologically recognized taxonomic groups (subfamilies) recovered with most representatives in one or a few contiguous groups or subclusters.
    Molecular Ecology Resources 04/2012; 12(4):676-85. · 3.06 Impact Factor
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    Article: Wolbachia and DNA barcoding insects: patterns, potential, and problems.
    [show abstract] [hide abstract]
    ABSTRACT: Wolbachia is a genus of bacterial endosymbionts that impacts the breeding systems of their hosts. Wolbachia can confuse the patterns of mitochondrial variation, including DNA barcodes, because it influences the pathways through which mitochondria are inherited. We examined the extent to which these endosymbionts are detected in routine DNA barcoding, assessed their impact upon the insect sequence divergence and identification accuracy, and considered the variation present in Wolbachia COI. Using both standard PCR assays (Wolbachia surface coding protein--wsp), and bacterial COI fragments we found evidence of Wolbachia in insect total genomic extracts created for DNA barcoding library construction. When >2 million insect COI trace files were examined on the Barcode of Life Datasystem (BOLD) Wolbachia COI was present in 0.16% of the cases. It is possible to generate Wolbachia COI using standard insect primers; however, that amplicon was never confused with the COI of the host. Wolbachia alleles recovered were predominantly Supergroup A and were broadly distributed geographically and phylogenetically. We conclude that the presence of the Wolbachia DNA in total genomic extracts made from insects is unlikely to compromise the accuracy of the DNA barcode library; in fact, the ability to query this DNA library (the database and the extracts) for endosymbionts is one of the ancillary benefits of such a large scale endeavor--which we provide several examples. It is our conclusion that regular assays for Wolbachia presence and type can, and should, be adopted by large scale insect barcoding initiatives. While COI is one of the five multi-locus sequence typing (MLST) genes used for categorizing Wolbachia, there is limited overlap with the eukaryotic DNA barcode region.
    PLoS ONE 01/2012; 7(5):e36514. · 4.09 Impact Factor
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    Article: Mariapanteles (Hymenoptera, Braconidae), a new genus of Neotropical microgastrine parasitoid wasp discovered through biodiversity inventory.
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    ABSTRACT: A new genus of microgastrine parasitoid wasps, Mariapanteles Whitfield & Fernández-Triana, gen. n., is described from rain forests of the Neotropics. The new genus is related to the common and speciose genus Pseudapanteles, but can be distinguished from the latter by having a complete transverse carina on the propodeum which forks around the spiracles. A molecular analysis based on data from COI from specimens of the proposed new genus plus possibly related genera confirms its generic distinctness. A key to two known species, Mariapanteles felipei Whitfield, sp. n. (Costa Rica) and Mariapanteles dapkeyae Fernández-Triana, sp. n. (Brazil) is provided. Evidence from collections suggests that there are other undescribed Neotropical congenerics. Specimens of Mariapanteles were likely confused in the past with the genus Beyarslania (referred to as Xenogaster until recently) but present information suggests that Beyarslania is restricted to the Afrotropical region while the Neotropical species clearly belong to a different genus, which we propose as new.
    ZooKeys 01/2012; · 0.88 Impact Factor
  • Article: A distinctive new species of Euglyphis Hübner (Lepidoptera: Lasiocampidae) from Costa Rica, with a checklist of the Euglyphis known from Costa Rica
    Jose Montero, Daniel H Janzen, Winnie Hallwachs
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    ABSTRACT: Euglyphis jessiehillae Montero, new species, is described from Costa Rican rain forest. Photographs of the adult, larva and cocoon, as well as male and female genitalia, are provided. In addition to its description and natural history, we include a checklist for the described members of the genus Euglyphis known from Costa Rica.
    Zootaxa 09/2011; 3020:49-59. · 0.93 Impact Factor
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    Article: When species matches are unavailable are DNA barcodes correctly assigned to higher taxa? An assessment using sphingid moths.
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    ABSTRACT: When a specimen belongs to a species not yet represented in DNA barcode reference libraries there is disagreement over the effectiveness of using sequence comparisons to assign the query accurately to a higher taxon. Library completeness and the assignment criteria used have been proposed as critical factors affecting the accuracy of such assignments but have not been thoroughly investigated. We explored the accuracy of assignments to genus, tribe and subfamily in the Sphingidae, using the almost complete global DNA barcode reference library (1095 species) available for this family. Costa Rican sphingids (118 species), a well-documented, diverse subset of the family, with each of the tribes and subfamilies represented were used as queries. We simulated libraries with different levels of completeness (10-100% of the available species), and recorded assignments (positive or ambiguous) and their accuracy (true or false) under six criteria. A liberal tree-based criterion assigned 83% of queries accurately to genus, 74% to tribe and 90% to subfamily, compared to a strict tree-based criterion, which assigned 75% of queries accurately to genus, 66% to tribe and 84% to subfamily, with a library containing 100% of available species (but excluding the species of the query). The greater number of true positives delivered by more relaxed criteria was negatively balanced by the occurrence of more false positives. This effect was most sharply observed with libraries of the lowest completeness where, for example at the genus level, 32% of assignments were false positives with the liberal criterion versus < 1% when using the strict. We observed little difference (< 8% using the liberal criterion) however, in the overall accuracy of the assignments between the lowest and highest levels of library completeness at the tribe and subfamily level. Our results suggest that when using a strict tree-based criterion for higher taxon assignment with DNA barcodes, the likelihood of assigning a query a genus name incorrectly is very low, if a genus name is provided it has a high likelihood of being accurate, and if no genus match is available the query can nevertheless be assigned to a subfamily with high accuracy regardless of library completeness. DNA barcoding often correctly assigned sphingid moths to higher taxa when species matches were unavailable, suggesting that barcode reference libraries can be useful for higher taxon assignments long before they achieve complete species coverage.
    BMC Ecology 08/2011; 11:18.
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    Article: Reading the complex skipper butterfly fauna of one tropical place.
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    ABSTRACT: An intense, 30-year, ongoing biodiversity inventory of Lepidoptera, together with their food plants and parasitoids, is centered on the rearing of wild-caught caterpillars in the 120,000 terrestrial hectares of dry, rain, and cloud forest of Area de Conservacion Guanacaste (ACG) in northwestern Costa Rica. Since 2003, DNA barcoding of all species has aided their identification and discovery. We summarize the process and results for a large set of the species of two speciose subfamilies of ACG skipper butterflies (Hesperiidae) and emphasize the effectiveness of barcoding these species (which are often difficult and time-consuming to identify). Adults are DNA barcoded by the Biodiversity Institute of Ontario, Guelph, Canada; and they are identified by correlating the resulting COI barcode information with more traditional information such as food plant, facies, genitalia, microlocation within ACG, caterpillar traits, etc. This process has found about 303 morphologically defined species of eudamine and pyrgine Hesperiidae breeding in ACG (about 25% of the ACG butterfly fauna) and another 44 units indicated by distinct barcodes (n = 9,094), which may be additional species and therefore may represent as much as a 13% increase. All but the members of one complex can be identified by their DNA barcodes. Addition of DNA barcoding to the methodology greatly improved the inventory, both through faster (hence cheaper) accurate identification of the species that are distinguishable without barcoding, as well as those that require it, and through the revelation of species "hidden" within what have long been viewed as single species. Barcoding increased the recognition of species-level specialization. It would be no more appropriate to ignore barcode data in a species inventory than it would be to ignore adult genitalia variation or caterpillar ecology.
    PLoS ONE 01/2011; 6(8):e19874. · 4.09 Impact Factor
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    Article: Joining inventory by parataxonomists with DNA barcoding of a large complex tropical conserved wildland in northwestern Costa Rica.
    Daniel H Janzen, Winnie Hallwachs
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    ABSTRACT: The many components of conservation through biodiversity development of a large complex tropical wildland, Area de Conservacion Guanacaste (ACG), thrive on knowing what is its biodiversity and natural history. For 32 years a growing team of Costa Rican parataxonomists has conducted biodiversity inventory of ACG caterpillars, their food plants, and their parasitoids. In 2003, DNA barcoding was added to the inventory process. We describe some of the salient consequences for the parataxonomists of barcoding becoming part of a field biodiversity inventory process that has centuries of tradition. From the barcoding results, the parataxonomists, as well as other downstream users, gain a more fine-scale and greater understanding of the specimens they find, rear, photograph, database and deliver. The parataxonomists also need to adjust to collecting more specimens of what appear to be the "same species"--cryptic species that cannot be distinguished by eye or even food plant alone--while having to work with the name changes and taxonomic uncertainty that comes with discovering that what looked like one species may be many. These career parataxonomists, despite their lack of formal higher education, have proven very capable of absorbing and working around the additional complexity and requirements for accuracy and detail that are generated by adding barcoding to the field base of the ACG inventory. In the process, they have also gained a greater understanding of the fine details of phylogeny, relatedness, evolution, and species-packing in their own tropical complex ecosytems. There is no reason to view DNA barcoding as incompatible in any way with tropical biodiversity inventory as conducted by parataxonomists. Their year-round on-site inventory effort lends itself well to the sampling patterns and sample sizes needed to build a thorough barcode library. Furthermore, the biological understanding that comes with barcoding increases the scientific penetrance of biodiversity information, DNA understanding, evolution, and ecology into the communities in which the parataxonomists and their families are resident.
    PLoS ONE 01/2011; 6(8):e18123. · 4.09 Impact Factor
  • Article: Lytopylus Förster (Hymenoptera, Braconidae, Agathidinae) species from Costa Rica, with an emphasis on specimens reared from caterpillars in Area de Conservación Guanacaste.
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    ABSTRACT: Twelve species of Costa Rican Lytopylus are treated; these include all species reared from Lepidoptera caterpillars in Area de Conservación Guanacaste, Costa Rica, over 32 years of caterpillar inventory, as well as two species recorded in the literature as occurring in Costa Rica. Ten new species are described, i.e., Lytopylus bradzlotnicki, Lytopylus colleenhitchcockae, Lytopylus gregburtoni, Lytopylus jessicadimauroae, Lytopylus jessiehillae, Lytopylus mingfangi, Lytopylus rebeccashapleyae, Lytopylus robpringlei, Lytopylus sandraberriosae, Lytopylus vaughntani. The following species are transferred to Lytopylus: Metriosoma flavicalcar Enderlein 1920 to Lytopylus flavicalcarcomb. n.; Bassus macadamiae Briceño and Sharkey 2000 to Lytopylus macadamiaecomb. n.; Metriosoma bicarinatum Enderlein 1920 to Lytopylus bicarinatumcomb. n.; Metriosoma brasiliense Enderlein 1920 to Lytopylus brasiliensecomb. n.; Bassus tayrona Campos 2007 to Lytopylus tayronacomb. n.; Microdus femoratus Cameron 1887 to Lytopylus femoratuscomb. n.; Microdus melanocephalus Cameron 1887 to Lytopylus melanocephaluscomb. n.; Bassus pastranai Blanchard 1952 to Lytopylus pastranaicomb. n.; Agathis nigrobalteata Cameron 1911 to Lytopylus nigrobalteatuscomb. n. Two keys to species of Lytopylus are presented, one interactive and the other static.
    ZooKeys 01/2011; · 0.88 Impact Factor
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    Article: Pyrosequencing for mini-barcoding of fresh and old museum specimens.
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    ABSTRACT: DNA barcoding is an effective approach for species identification and for discovery of new and/or cryptic species. Sanger sequencing technology is the method of choice for obtaining standard 650 bp cytochrome c oxidase subunit I (COI) barcodes. However, DNA degradation/fragmentation makes it difficult to obtain a full-length barcode from old specimens. Mini-barcodes of 130 bp from the standard barcode region have been shown to be effective for accurate identification in many animal groups and may be readily obtained from museum samples. Here we demonstrate the application of an alternative sequencing technology, the four-enzymes single-specimen pyrosequencing, in rapid, cost-effective mini-barcode analysis. We were able to generate sequences of up to 100 bp from mini-barcode fragments of COI in 135 fresh and 50 old Lepidoptera specimens (ranging from 53-97 year-old). The sequences obtained using pyrosequencing were of high quality and we were able to robustly match all the tested pyro-sequenced samples to their respective Sanger-sequenced standard barcode sequences, where available. Simplicity of the protocol and instrumentation coupled with higher speed and lower cost per sequence than Sanger sequencing makes this approach potentially useful in efforts to link standard barcode sequences from unidentified specimens to known museum specimens with only short DNA fragments.
    PLoS ONE 01/2011; 6(7):e21252. · 4.09 Impact Factor
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    Article: A tropical horde of counterfeit predator eyes.
    Daniel H Janzen, Winnie Hallwachs, John M Burns
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    ABSTRACT: We propose that the many different, but essentially similar, eye-like and face-like color patterns displayed by hundreds of species of tropical caterpillars and pupae-26 examples of which are displayed here from the dry, cloud, and rain forests of Area de Conservacion Guanacaste (ACG) in northwestern Costa Rica-constitute a huge and pervasive mimicry complex that is evolutionarily generated and sustained by the survival behavior of a large and multispecific array of potential predators: the insect-eating birds. We propose that these predators are variously and innately programmed to flee when abruptly confronted, at close range, with what appears to be an eye of one of their predators. Such a mimetic complex differs from various classical Batesian and Müllerian mimicry complexes of adult butterflies in that (i) the predators sustain it for the most part by innate traits rather than by avoidance behavior learned through disagreeable experiences, (ii) the more or less harmless, sessile, and largely edible mimics vastly outnumber the models, and (iii) there is no particular selection for the eye-like color pattern to closely mimic the eye or face of any particular predator of the insect-eating birds or that of any other member of this mimicry complex. Indeed, selection may not favor exact resemblance among these mimics at all. Such convergence through selection could create a superabundance of one particular false eyespot or face pattern, thereby increasing the likelihood of a bird species or guild learning to associate that pattern with harmless prey.
    Proceedings of the National Academy of Sciences 06/2010; 107(26):11659-65. · 9.68 Impact Factor
  • Article: Of Many Similar Species in the Neotropical Genus Porphyrogenes (Lepidoptera: Hesperiidae), a New One, Repeatedly Reared in Costa Rica, is Relatively Distinct
    John M. Burns, Daniel H. Janzen, Winnie Hallwachs
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    ABSTRACT: Associating sexes in many species of the Neotropical hesperiid genus Porphyrogenes has been difficult, erroneous, or impossible, owing to their sexual dimorphism. Despite the extreme sexual dimorphism of Porphyrogenes peterwegei Burns, new species, full description of this rainforest skipper from Area de Conservación Guanacaste (ACG), northwestern Costa Rica, is no problem. The available sample amounts to nearly 100 reared adults, almost evenly divided between the sexes. Of these, 67 have been DNA barcoded and found to vary minimally in their COI haplotypes, with one haplotype predominating. Caterpillars and pupae consistently go through a distinctive set of developmental changes in their color patterns. Foodplant choice is conservative: of 227 immatures found in the wild, 94% were eating woody vines of the genus Machaerium, especially M. seemannii (Fabaceae), whereas 6% were feeding on the quite unrelated species Dichapetalum morenoi (Dichapetalaceae)—a peculiar pattern of larval foodplant selection seen in another skipper and two butterfly species in ACG. Caterpillars of P. peterwegei are occasionally attacked by a host-specific parasitoid (an undescribed tachinid of the genus Siphosturmia), which has not otherwise been encountered in 20,642 tachinid attacks on the caterpillars of >3,000 species of Lepidoptera in ACG. Morphologically, P. peterwegei differs significantly from its many congeners in both facies and genitalia.
    Proceedings- Entomological Society of Washington 02/2010; · 0.40 Impact Factor
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    Article: Integration of DNA barcoding into an ongoing inventory of complex tropical biodiversity.
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    ABSTRACT: Inventory of the caterpillars, their food plants and parasitoids began in 1978 for today's Area de Conservacion Guanacaste (ACG), in northwestern Costa Rica. This complex mosaic of 120 000 ha of conserved and regenerating dry, cloud and rain forest over 0-2000 m elevation contains at least 10 000 species of non-leaf-mining caterpillars used by more than 5000 species of parasitoids. Several hundred thousand specimens of ACG-reared adult Lepidoptera and parasitoids have been intensively and extensively studied morphologically by many taxonomists, including most of the co-authors. DNA barcoding - - the use of a standardized short mitochondrial DNA sequence to identify specimens and flush out undisclosed species - - was added to the taxonomic identification process in 2003. Barcoding has been found to be extremely accurate during the identification of about 100 000 specimens of about 3500 morphologically defined species of adult moths, butterflies, tachinid flies, and parasitoid wasps. Less than 1% of the species have such similar barcodes that a molecularly based taxonomic identification is impossible. No specimen with a full barcode was misidentified when its barcode was compared with the barcode library. Also as expected from early trials, barcoding a series from all morphologically defined species, and correlating the morphological, ecological and barcode traits, has revealed many hundreds of overlooked presumptive species. Many but not all of these cryptic species can now be distinguished by subtle morphological and/or ecological traits previously ascribed to 'variation' or thought to be insignificant for species-level recognition. Adding DNA barcoding to the inventory has substantially improved the quality and depth of the inventory, and greatly multiplied the number of situations requiring further taxonomic work for resolution.
    Molecular Ecology Resources 04/2009; 9(S1):1-26. · 3.06 Impact Factor
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    Article: Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections.
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    ABSTRACT: We DNA barcoded 2,597 parasitoid wasps belonging to 6 microgastrine braconid genera reared from parapatric tropical dry forest, cloud forest, and rain forest in Area de Conservación Guanacaste (ACG) in northwestern Costa Rica and combined these data with records of caterpillar hosts and morphological analyses. We asked whether barcoding and morphology discover the same provisional species and whether the biological entities revealed by our analysis are congruent with wasp host specificity. Morphological analysis revealed 171 provisional species, but barcoding exposed an additional 142 provisional species; 95% of the total is likely to be undescribed. These 313 provisional species are extraordinarily host specific; more than 90% attack only 1 or 2 species of caterpillars out of more than 3,500 species sampled. The most extreme case of overlooked diversity is the morphospecies Apanteles leucostigmus. This minute black wasp with a distinctive white wing stigma was thought to parasitize 32 species of ACG hesperiid caterpillars, but barcoding revealed 36 provisional species, each attacking one or a very few closely related species of caterpillars. When host records and/or within-ACG distributions suggested that DNA barcoding had missed a species-pair, or when provisional species were separated only by slight differences in their barcodes, we examined nuclear sequences to test hypotheses of presumptive species boundaries and to further probe host specificity. Our iterative process of combining morphological analysis, ecology, and DNA barcoding and reiteratively using specimens maintained in permanent collections has resulted in a much more fine-scaled understanding of parasitoid diversity and host specificity than any one of these elements could have produced on its own.
    Proceedings of the National Academy of Sciences 09/2008; 105(34):12359-64. · 9.68 Impact Factor
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    Article: DNA barcodes and cryptic species of skipper butterflies in the genus Perichares in Area de Conservacion Guanacaste, Costa Rica.
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    ABSTRACT: DNA barcodes can be used to identify cryptic species of skipper butterflies previously detected by classic taxonomic methods and to provide first clues to the existence of yet other cryptic species. A striking case is the common geographically and ecologically widespread neotropical skipper butterfly Perichares philetes (Lepidoptera, Hesperiidae), described in 1775, which barcoding splits into a complex of four species in Area de Conservación Guanacaste (ACG) in northwestern Costa Rica. Three of the species are new, and all four are described. Caterpillars, pupae, and foodplants offer better distinguishing characters than do adults, whose differences are mostly average, subtle, and blurred by intraspecific variation. The caterpillars of two species are generalist grass-eaters; of the other two, specialist palm-eaters, each of which feeds on different genera. But all of these cryptic species are more specialized in their diet than was the morphospecies that held them. The four ACG taxa discovered to date belong to a panneotropical complex of at least eight species. This complex likely includes still more species, whose exposure may require barcoding. Barcoding ACG hesperiid morphospecies has increased their number by nearly 10%, an unexpectedly high figure for such relatively well known insects.
    Proceedings of the National Academy of Sciences 05/2008; 105(17):6350-5. · 9.68 Impact Factor
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    Article: DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists.
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    ABSTRACT: Many species of tachinid flies are viewed as generalist parasitoids because what is apparently a single species of fly has been reared from many species of caterpillars. However, an ongoing inventory of the tachinid flies parasitizing thousands of species of caterpillars in Area de Conservación Guanacaste, northwestern Costa Rica, has encountered >400 species of specialist tachinids with only a few generalists. We DNA-barcoded 2,134 flies belonging to what appeared to be the 16 most generalist of the reared tachinid morphospecies and encountered 73 mitochondrial lineages separated by an average of 4% sequence divergence. These lineages are supported by collateral ecological information and, where tested, by independent nuclear markers (28S and ITS1), and we therefore view these lineages as provisional species. Each of the 16 apparently generalist species dissolved into one of four patterns: (i) a single generalist species, (ii) a pair of morphologically cryptic generalist species, (iii) a complex of specialist species plus a generalist, or (iv) a complex of specialists with no remaining generalist. In sum, there remained 9 generalist species among the 73 mitochondrial lineages we analyzed, demonstrating that a generalist lifestyle is possible for a tropical caterpillar parasitoid fly. These results reinforce the emerging suspicion that estimates of global species richness are likely underestimates for parasitoids (which may constitute as much as 20% of all animal life) and that the strategy of being a tropical generalist parasitic fly may be yet more unusual than has been envisioned for tachinids.
    Proceedings of the National Academy of Sciences 03/2007; 104(12):4967-72. · 9.68 Impact Factor