Morphological and Genetic Reappraisal of the Orius Fauna of the Western United States (Hemiptera: Heteroptera: Anthocoridae)
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Annals of the Entomological Society of America, 109(2), 2016, 319–334 doi: 10.1093/aesa/sav155 Advance Access Publication Date: 7 January 2016 Systematics Research article Morphological and Genetic Reappraisal of the Orius Fauna of the Western United States (Hemiptera: Heteroptera: Anthocoridae) David R. Horton, Tamera M. Lewis, Stephen F. Garczynski, Kelly Thomsen-Archer, and Thomas R. Unruh Downloaded from https://academic.oup.com/aesa/article/109/2/319/2195305 by guest on 23 September 2021 USDA-ARS, 5230 Konnowac Pass Rd., Wapato, WA 98951 ([email protected]; [email protected]; steve. [email protected]; [email protected]; [email protected]) and 1Corresponding author, e-mail: [email protected] Received 27 August 2015; Accepted 8 December 2015 Abstract Examination of minute pirate bugs, Orius spp. (Hemiptera: Heteroptera: Anthocoridae), from a broad geo- graphic range in the western United States prompted a reappraisal of the taxonomic composition of the fauna native to the western United States and Canada. Current syntheses and catalogs list three species of Orius na- tive to this region. In a previous study, we showed how geographic variation in external traits of one of these species, Orius diespeter Herring, 1966, had led to mistakes in identification of species within this complex. More extensive collecting efforts have now led to the discovery of specimens having traits not fully consistent with descriptions of any described species. We provisionally categorized these unresolved specimens into one of eight phenotypic groups based upon combinations of body size, visual appearance of genitalia, association with specific plant taxa, and geographic source. Genitalia from 382 specimens were then measured to deter- mine whether phenotypic groupings were confirmed by statistical analysis of genitalic morphology. Principal components analysis showed that size and shape of the male’s paramere differed among phenotypes. The par- amere of unresolved specimens often diverged from the paramere of described species. Length of the female’s copulatory tube differed between several of the unresolved phenotypes and described species. Analysis of DNA sequences showed that five of the eight phenotypes diverged genetically from other phenotypes and from de- scribed species. DNA sequence data did not separate two described species (Orius tristicolor (White, 1879) and Orius harpocrates Herring, 1966), suggesting that these two species are a single species. The combined mor- phological and genetic evidence indicates that the Orius fauna of the western United States is composed of a mix of two described species and possibly five undescribed cryptic species. We summarize the known distribu- tions of described and cryptic undescribed species, and discuss the implications of our work for the biological control community. Key words: Orius, genitalia, mtDNA, cryptic species Insects in the Family Anthocoridae (Hemiptera: Heteroptera) are Hawaii (Davis and Krauss 1963) as components of classical biologi- predators of small soft-bodied arthropods in crop and natural sys- cal control attempts. tems worldwide (Lattin 1999). In the continental United States and In many areas worldwide, the Orius fauna is composed of com- Canada, the Anthocoridae includes about 90 species (Henry 1988), plexes of often highly similar species. These complexes may occupy of which members of the genus Orius Wolff, 1811, are the most the same agricultural fields, stands of vegetation, or even the same familiar. There are 70 known species of Orius worldwide individual plant (e.g., Knowlton 1949, Lykouressis and Perdikis (Yasunaga 1997). Species of Orius are important sources of biologi- 1997, Ohno and Takemoto 1997, Lewis et al. 2005, Shapiro et al. cal control on row crops, in greenhouses, and on flowering orna- 2009, Lewis and Horton 2010). Because life histories and impact on mentals (Lattin 1999). Several species of Orius are reared prey almost certainly vary species-to-species within complexes (Ito commercially for release in North America and Europe (Cranshaw and Nakata 1998, Tommasini et al. 2004), it is important that spe- et al. 1996, van Lenteren et al. 1997). North American species of cies within complexes are correctly identified. Similarity in appear- Orius have been released in Europe (Tommasini et al. 2004) and ance among species in some Orius complexes can make it very Published by Oxford University Press on behalf of Entomological Society of America 2016. This work is written by US Government employees and is in the public domain in the US. 319 320 Annals of the Entomological Society of America, 2016, Vol. 109, No. 2 difficult to separate them, and mistakes in identification are not size, visual appearance of genitalia, plant source, and geographic uncommon (e.g., Shapiro and Ferkovich 2009, Lewis and Horton source. We then measured genitalia of a subset of identified and 2010, Lewis and Lattin 2010). unresolved specimens, and examined whether size and shape of geni- The two senior authors of this paper recently conducted an talia differed among phenotypes or between unresolved phenotypes extensive reevaluation of the morphology and geographic distribu- and described species. Lastly, we determined whether phenotypic tion of a North American species of minute pirate bug, Orius dies- groupings were consistent with differences among groups in DNA peter Herring, 1966 (Lewis and Horton 2010). Several hundred sequences. Variation in morphology of genitalia accompanied by specimens of Orius from throughout North America were examined clear differences in DNA sequences would be evidence for the exis- in that study, and it became clear from those specimens that the tence of a cryptic species complex within the North American fauna Orius complex in western North America includes insects whose of Orius. external traits and genitalic morphology are not fully consistent with descriptions of O. diespeter or other described species. The dis- crepancies between literature descriptions and specimens were often Genitalia of Orius Downloaded from https://academic.oup.com/aesa/article/109/2/319/2195305 by guest on 23 September 2021 quite subtle, and a number of specimens whose external appearance An important structure for identifying species of Orius is the left identified them as either O. diespeter or a common western species, paramere of the male, which has been used in taxonomic treatments Orius tristicolor (White, 1879), were found upon examination of of Orius beginning with the work of Ribaut (1923). As in other male or female genitalia to depart from descriptions of genitalia Anthocoridae, the right paramere has been lost, while the left func- available in earlier publications. tions as a copulatory organ (Carayon 1972, Pe´ricart 1972). The scle- These observations prompted us to conduct a quantitative rotized organ is situated in a small recessed area on the dorsal part examination of genitalic morphology for the Orius fauna native to of the male’s ninth abdominal segment (Fig. 1A). During mating, the western North America. We examined Orius collected from male extends his abdomen beneath the female, and rotates the para- throughout the western half of the United States, with more limited mere until the flagellum and associated, membranous endosoma can collecting of specimens from the southcentral and southeastern part be inserted into the female’s genitalia. The paramere is a complex, of the country. Specimens that could not readily be identified as three-dimensional structure, accompanied on its dorsal surface by described species by descriptions and illustrations in the literature an apically tapered cone and flagellum (Fig. 1A). The cone and flag- (White 1879; Kelton 1963, 1978; Herring 1966; Lewis and Horton ellum often differ in appearance among species, and the two struc- 2010) were assigned provisionally to one of eight phenotypic tures are used extensively in taxonomic treatments of Orius. In groups. These groups were delineated by a combination of body some especially difficult complexes, species cannot be identified Fig. 1. (A) Abdomen and paramere (in dorsal view) of two Old World species of Orius (after Yasunaga 1997); (B) copulatory tube of O. tristicolor (in dorsal view); and (C) photograph of the copulatory tube of O. tristicolor showing thickened basal region and membranous region terminating in sperm pouch (in dorsal view). Annals of the Entomological Society of America, 2016, Vol. 109, No. 2 321 without examination of parameres (Ghauri 1972, Pe´ricart 1972, misidentifications of specimens (Fig. 3A; see the discussion of Yasunaga 1997, Lewis and Horton 2010). O. diespeter below). Less often, morphology of the female’s genitalia is used to identify The taxonomic status of O. tristicolor was uncertain throughout species of Orius (Pe´ricart 1972, Yasunaga 1997, Postle et al. 2001, the late 1800s and first half of the 1900s, due to questions about Lewis and Horton 2010). A specialized structure (copulatory tube; whether White had described a valid species or whether the species Carayon 1953) of female Orius acts to receive the genitalia of the was merely a color variant of the common eastern minute pirate male and to channel the male’s intromittent organ to the sperm stor- bug, Orius insidiosus (Say, 1832). Indeed, many early 1900s cita- age organ located at the terminal end of her copulatory tube (Fig. 1B tions actually refer to O. tristicolor as a color variant of O. insidio- and C). The structure opens