Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxys koreanus Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae)

Authors: DESNEUX, NICOLAS - Institute National De La Recherche Agronomique De Tunisie (INRAT); STARY, PETR - Academy Of Science Of Czech Republic; DELEBECQUE, CAMILLE - University Of Minnesota; GARIEPY, TARA - University Of Hawaii; BARTA, RUTH - University Of Minnesota; Hoelmer, Kim; HEIMPEL, GEORGE - University Of Minnesota

Submitted to: Annals of the Entomological Society of America
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/18/2009
Publication Date: 11/10/2009
Citation: Desneux, N., Stary, P., Delebecque, C.J., Gariepy, T.D., Barta, R.J., Hoelmer, K.A., Heimpel, G.E. 2009. Cryptic species of parasitoids attacking the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), in Asia: Binodoxys communis Gahan and Binodoxys koreanus Stary sp. n. (Hymenoptera: Braconidae: Aphidiinae). Annals of the Entomological Society of America. 102(6):925-936.

Interpretive Summary: The invasive soybean aphid, a native of northeast Asian countries, infests soybean fields in North America and is a serious pest throughout soybean-growing areas of the Midwest. While parasitic wasps ("parasitoids") exert substantial control of soybean aphid in Asian countries, surveys have shown that native wasps attacking soybean aphid in North America are less effective. Initial biological control efforts directed at the soybean aphid have resulted in the importation of several aphid natural enemies from China, Japan and South Korea into US quarantine laboratories. Collections of parasitoids attacking soybean aphid in Korea yielded a population originally identified as Binodoxys communis, a common Asian soybean aphid parasitoid. Our studies showed that this population is actually a separate, previously unknown species of Binodoxys. These studies included mating trials, genetic analysis, comparisons of host-use patterns and examination of physical characteristics in both populations. We propose the name Binodoxys koreanus Stary sp. n. for the Korean population. Both species of Binodoxys have similar host ranges, except that B. koreanus sp. n. is better able to develop in a population of the cow-pea aphid, Aphis craccivora. Further studies are required to determine whether the new species would effectively complement ongoing biological control efforts.

Technical Abstract: Collections of parasitoids attacking the soybean aphid, Aphis glycines, in Korea yielded a population that was originally identified as Binodoxys communis Gahan (Hymenoptera; Braconidae: Aphidiinae) based upon current identification keys. Our laboratory studies indicated that this population is actually a separate, previously unknown species of Binodoxys. These studies consisted of four classes of comparisons between the Korean population of Binodoxys and a Chinese population that had also been identified as B. communis. The comparisons included (i) mating trials coupled with behavioral observations and spermathecal examination, (ii) assessment of nucleotide divergence at two mitochondrial and two nuclear genes, (iii) comparisons of host-use patterns between the Korean and Chinese population of Binodoxys and (iv) a re-assessment of morphological characters of both populations. These studies indicated pre-mating reproductive isolation and minor nucleotide differences in mitochondrial COI sequences and nuclear ITS1 sequences between the two populations, which suggests strongly that they are different species. Subtle morphological differences were also discovered that confirmed that the Chinese population belongs to B. communis while the Korean population does not. We propose the name Binodoxys koreanus Stary sp. n. for the Korean population. We compared host use patterns by offering females of the two species 20 aphid species separately in oviposition trials. This study indicated similar host ranges, with the most notable exception being that B. koreanus sp. n. is better able to develop in a population of Aphis craccivora that harbors a bacterial endosymbiont, Hamiltonella defensa, which appears to strongly interfere with development of B. communis. We discuss the implications of our results for biological control of the soybean aphid.