Cyclical parthenogenetic reproduction in the Russian wheat aphid (Hemiptera: Aphididae) in the United States: sexual reproduction and its outcome on biotypic diversity.

In 1986, the Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Hemiptera: Aphididae), became an invasive species of United States. Nearly 20 yr later, new biotypes appeared that were capable of overcoming most sources of resistance and became a renewed threat to wheat, Triticum aestivum L., production. Cyclical (CP) and obligate (OP) parthenogenesis enables aphids to both adapt to changing environments and exploit host resources. We documented these forms of reproduction for Russian wheat aphid in wheat and wild grasses in the Central Great Plains and Rocky Mountain regions during falls 2004-2009. Colonies from sample sites also were held under unheated greenhouse conditions and observed for the presence of sexual morphs and eggs through the winter. Russian wheat aphid populations were mainly OP and attempted to overwinter as adults, regardless of region sampled. A few populations contained oviparae but no males (gynocyclic) and were not specific to any particular region. Observation of the Russian wheat aphid colonies under greenhouse conditions failed to produce males or eggs. In spring 2007, CP was confirmed in a small population of Russian wheat aphid that eclosed from eggs (fundatricies) on wild grasses and wheat near Dove Creek, CO, in the Colorado Plateau region where other aphid species undergo CP. Lineages from ninety-three fundatricies were screened against 16 resistant and susceptible cereal entries to determine their biotypic classification. A high degree of biotypic diversity (41.4%) was detected in this population. Although CP was a rare in Russian wheat aphid populations, genetic recombination during the sexual cycle creates new biotypes and can have significant effects on population genetics.

Biology and biotype determination of greenbug, Schizaphis graminum (Hemiptera: Aphididae), on seashore paspalum turfgrass (Paspalum vaginatum).

Greenbug, Schizaphis graminum (Rondani) (Hemiptera: Aphididae), was first discovered damaging seashore paspalum (Paspalum vaginatum Swartz) turfgrass in November 2003 at Belle Glade, FL. Inquiries to several golf courses with seashore paspalum turf across southern Florida indicated infestation was wide spread by April 2004. Damage symptoms progress from water soaked lesions surrounding feeding sites within 24 h to chlorosis and necrosis of leaf tips within 96 h. Problems caused by greenbug feeding were initially misdiagnosed as fertilizer, disease, other insects, or water management problems because aphids were not previously found on warm season turfgrasses. Greenbug development and fecundity studies were conducted on six seashore paspalum varieties: 'Aloha,' 'SeaDwarf,' 'SeaGreen,' 'SeaIsle,' 'SeaWay,' and 'SeaWolf.' Greenbug did not survive on 'SeaWolf.' Development rates (mean +/- SEM) ranged from 7.6 +/- 0.2 to 8.2 +/- 0.2 d on the remaining varieties. Greenbug longevity and fecundity on 'Aloha' were significantly less than on the other varieties. The estimated intrinsic rate of natural increase (r(m)) for greenbug ranged from 0.24 to 0.26 across tested varieties. Values for net reproductive rate (R(o)) ranged from 12.3 on 'Aloha' to 40.4 on 'SeaWay.' In feeding trials on indicator plants, the Florida isolate of greenbug exhibited a unique biotypic profile most commonly found on noncultivated grass hosts. It was virulent on the wheat variety GRS1201 that is resistant to the principal agricultural biotypes attacking small grains and to all currently available resistant sorghum varieties.

Response of resistant and susceptible barley to infestations of five Diuraphis noxia (Homoptera: Aphididae) biotypes.

Since 2003, four new biotypes of the Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae), RWA2-RWA5, have been discovered that have the ability to damage most of the wheat germplasm resistant to the original Russian wheat aphid population (RWA1). Barley germplasm lines with resistance to RWA1 have not yet been evaluated against the newest biotypes. Our study compared how biotypes RWA1-RWA5 affected the growth and leaf damage of RWA1-resistant germplasm (STARS 9301B, STARS 9577B), moderately resistant germplasm (MR-015), and susceptible varieties (Schuyler, Harrington, and Morex) under greenhouse conditions. Russian wheat aphid population levels also were determined 14 d after plant infestation. STARS 9301B exhibited strong resistance by showing only small differences in leaf damage and growth parameters from the feeding by the biotypes. STARS 9577B showed greater differences in damage by the Russian wheat aphid biotypes than STARS 9301B, yet, the ratings were still within the resistant category (e.g., chlorosis rating 2.3-4.9). Leaf chlorosis ratings for MR-015 ranged from 5.0 to 6.9 and fell within the moderately resistant to susceptible categories for all the biotypes. The greatest difference in leaf chlorosis occurred in Morex where RWA2 showed less virulence than the other biotypes. Feeding by the Russian wheat aphid biotypes produced only small differences in leaf rolling and plant growth within plant entries. Population levels of the Russian wheat aphid biotypes did not differ within barley entries (n = 610-971) at the termination of the study (14 d). From our research, we conclude that the new Russian wheat aphid biotypes pose no serious threat to the key sources of resistance in barley (STARS 9301B and 9577B).

Mitochondrial DNA sequence divergence among Schizaphis graminum (Hemiptera: Aphididae) clones from cultivated and non-cultivated hosts: haplotype and host associations.

A 1.0 kb region of the mitochondrial cytochrome oxidase subunit I gene from the greenbug aphid, Schizaphis graminum (Rondani), was sequenced for 24 field collected clones from non-cultivated and cultivated hosts. Maximum likelihood, maximum parsimony and neighbour-joining phylogenies were estimated for these clones, plus 12 previously sequenced clones. All three tests produced trees with identical topologies and confirmed the presence of three clades within S. graminum. Clones showed no relationship between biotype and mtDNA haplotype. At least one biotype was found in all three clades, suggesting exchange among clades of genetic material conditioning for crop virulence, or the sharing of a common ancestor. However, there was a relationship between host and haplotype. Clade 1 was the most homogeneous and contained 12 of 16 clones collected from cultivated hosts and five of the six collected from johnsongrass, Sorghum halepense, a congener of cultivated sorghum, S. bicolor. Four of the six clones collected from Agropyron spp. were found in clade 2. Clade 3 contained two clones from wheat, Triticum aestivum, and four from non-cultivated hosts other than Agropyron spp. A partitioning of populations by mtDNA haplotype and host suggests the occurrence of host adapted races in Schizaphis graminum.

Efficacy of pyramiding greenbug (Homoptera: Aphididae) resistance genes in wheat.

Durable resistance to greenbug, Schizaphis graminum (Rondani), in wheat is a goal of wheat improvement teams, and one that has been complicated by the regular occurrence of damaging biotypes. Simulation modeling studies suggest that pyramiding resistance genes, i.e., combining more than one resistance gene in a single cultivar or hybrid, may provide more durable resistance than sequential releases of single genes. We examined this theory by pyramiding resistance genes in wheat and testing a series of greenbug biotypes. Resistance genes Gb2, Gb3, and Gb6, and pyramided genes Gb2/Gb3, Gb2/Gb6, and Gb3/Gb6 were tested for effectiveness against biotypes E, F, G, H, and I. By comparing reactions of plants with pyramided genes to those with single resistance genes, we found that pyramiding provided no additional protection over that conferred by the single resistance genes. Based on the results of this test, we concluded that the sequential release of single resistance genes, combined with careful monitoring of greenbug population biotypes, is the most effective gene deployment strategy for greenbug resistance in wheat.

Relative suitability of crested wheatgrass and other perennial grass hosts for the Russian wheat aphid (Homoptera: Aphididae).

The Russian wheat aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), reproduces parthenogenetically in North America and must survive year-round on host plants, including in late summer when small grains are not in cultivation. During this time, cool-season perennial wheatgrasses (Poaceae: Triticeae) contribute substantially to aphid survival, crested wheatgrass (Agropyron spp.) particularly. In greenhouse studies, the number of aphids per plant was measured after four infestation periods on unvernalized and vernalized wheatgrasses. Before placement on these test plant species, aphids were reared either on winter wheat or on the grass host species on which aphid progeny were counted. On vernalized plants, aphids reared on wheat resulted in more aphids per test plant than when the aphids were reared on wheatgrasses, but on unvernalized plants the number of aphids per test plant did not differ significantly regardless of rearing host. Aphids on crested wheatgrass were similar in number to the other grasses when plants were unvernalized. However, when plants were vernalized, crested wheatgrass supported significantly more aphids than some of the other hosts. Aphid numbers increased on all test species as infestation period lengthened, and plant growth was largely unaffected by aphid feeding. These results suggest if sufficient moisture is available during summer when small grains are not in cultivation, all host species observed are capable of sustaining aphids. Crested wheatgrass is an abundant and important host of the Russian wheat aphid in its northern range of the western United States, but other less prevalent wheatgrasses also may contribute to aphid survival during late summer when small grains are not in cultivation.

Mitochondrial DNA sequence divergence among greenbug (Homoptera: aphididae) biotypes: evidence for host-adapted races.

The full complement of known greenbug, Schizaphis graminum (Rondani), biotypes found in the USA were subjected to a molecular phylogenetic analysis based on a 1.2-kb portion of the cytochrome oxidase I mitochondrial gene. In addition to these nine biotypes (B, C, E, F, G, H, I, J and K), a probable isolate of the enigmatic biotype A (NY), a 'new biotype' collected from Elymus canadensis (L.) (CWR), and an isolate from Germany (EUR) were included. Schizaphis rotundiventris (Signoret) was included as an outgroup. Genetic distances among S. graminum biotypes ranged from 0.08% to 6.17% difference in nucleotide substitutions. Neighbour-joining, maximum parsimony and maximum likelihood analyses all produced dendrograms revealing three clades within S. graminum. Clade 1 contained the 'agricultural' biotypes commonly found on sorghum and wheat (C, E, K, I, plus J) and there were few substitutions among these biotypes. Clade 2 contained F, G and NY, and Clade 3 contained B, CWR and EUR, all of which are rarely found on crops. The rarest biotype, H, fell outside the above clades and may represent another Schizaphis species. S. graminum biotypes are a mixture of genotypes belonging to three clades and may have diverged as host-adapted races on wild grasses.