The Endosymbiont Arsenophonus Is Widespread in Soybean Aphid, Aphis glycines, but Does Not Provide Protection from Parasitoids or a Fungal Pathogen

Abstract

Aphids commonly harbor bacterial facultative symbionts that have a variety of effects upon their aphid hosts, including defense against hymenopteran parasitoids and fungal pathogens. The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is infected with the symbiont Arsenophonus sp., which has an unknown role in its aphid host. Our research goals were to document the infection frequency and diversity of the symbiont in field-collected soybean aphids, and to determine whether Arsenophonus is defending soybean aphid against natural enemies. We performed diagnostic PCR and sequenced four Arsenophonus genes in soybean aphids from their native and introduced range to estimate infection frequency and genetic diversity, and found that Arsenophonus infection is highly prevalent and genetically uniform. To evaluate the defensive role of Arsenophonus, we cured two aphid genotypes of their natural Arsenophonus infection through ampicillin microinjection, resulting in infected and uninfected isolines within the same genetic background. These isolines were subjected to parasitoid assays using a recently introduced biological control agent, Binodoxys communis [Braconidae], a naturally recruited parasitoid, Aphelinus certus [Aphelinidae], and a commercially available biological control agent, Aphidius colemani [Braconidae]. We also assayed the effect of the common aphid fungal pathogen, Pandora neoaphidis (Remaudiere & Hennebert) Humber (Entomophthorales: Entomophthoraceae), on the same aphid isolines. We did not find differences in successful parasitism for any of the parasitoid species, nor did we find differences in P. neoaphidis infection between our treatments. Our conclusion is that Arsenophonus does not defend its soybean aphid host against these major parasitoid and fungal natural enemies.

Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection

“…For example, laboratory experiments suggested that X‐Type does not provide any detectable benefit to the pea aphid, but it is quite frequent and positively associated to H. defensa , suggesting it might have benefited from hitchhiking during the spread of H. defensa (Doremus & Oliver, ). Also, Wulff, Buckman, Wu, Heimpel, and White () did not find that the symbiont Arsenophonus was protecting its Aphis glycines host against its main parasites, but it was present at high frequency. This discrepancy between observation and expectation motivated further experiments revealing that Arsenophonus provides a general – yet to be described – benefit to the aphid (Wulff & White, ).…”

Stress‐induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid

“…Wulff et al. (2013) previously used fbaA, ftsK, yaeT , and the 23s‐16s rRNA for MLST analysis of Arsenophonus from soybean aphids. Additionally, we included the spoT gene using primers published by Jousselin et al.…”

“…In native and invasive soybean aphid populations the frequency of Arsenophonus is widespread (Wulff et al. 2013; Bansal et al. 2014a), but does not appear to confer resistance to parasitoids or fungal pathogens based on research comparing artificially cured versus infected individuals (Wulff et al.…”

“…2014a), but does not appear to confer resistance to parasitoids or fungal pathogens based on research comparing artificially cured versus infected individuals (Wulff et al. 2013). Recent work also found a general fitness benefit associated with Arsenophonus infection, but no evidence this symbiont is the primary factor driving phenotypic differences in aphid virulence to soybean plant defenses (Wulff and White 2015).…”

The natural occurrence of secondary bacterial symbionts in aphids

“…() on more than 80 aphid species (mostly on samples collected in France, Europe) found Arsenophonus to infect only five species ( Aphis craccivora, Aphis idaei van der Goot, 1912, Aphis spiraecola Patch, 1914, Aphis ruborum (Borner, 1932) and Melanaphis donacis (Passerini, 1862); Table S2, File S1). Additionally, other studies have detected Arsenophonus in A. gossypii in Africa and North America (Carletto et al ., ; Jones et al ., ); Aphis glycines Matsumura in North America and Asia (Wille & Hartman, ; Wulff et al ., ; Bansal et al ., ) and Aphis melosae Mier Durante & Ortego, 1999 in South America (Arneodo & Ortego, ). A study by Burke et al .…”