A major-effect genetic locus, ApRVII, controlling resistance against both adapted and non-adapted aphid biotypes in pea.

KEY MESSAGE: A genome-wide association study for pea resistance against a pea-adapted biotype and a non-adapted biotype of the aphid, Acyrthosiphon pisum, identified a genomic region conferring resistance to both biotypes. In a context of reduced insecticide use, the development of cultivars resistant to insect pests is crucial for an integrated pest management. Pea (Pisum sativum) is a crop of major importance among cultivated legumes, for the supply of dietary proteins and nitrogen in low-input cropping systems. However, yields of the pea crop have become unstable due to plant parasites. The pea aphid (Acyrthosiphon pisum) is an insect pest species forming a complex of biotypes, each one adapted to feed on one or a few related legume species. This study aimed to identify resistance to A. pisum and the underlying genetic determinism by examining a collection of 240 pea genotypes. The collection was screened against a pea-adapted biotype and a non-adapted biotype of A. pisum to characterize their resistant phenotype. Partial resistance was observed in some pea genotypes exposed to the pea-adapted biotype. Many pea genotypes were completely resistant to non-adapted biotype, but some exhibited partial susceptibility. A genome-wide association study, using pea exome-capture sequencing data, enabled the identification of the major-effect quantitative trait locus ApRVII on the chromosome 7. ApRVII includes linkage disequilibrium blocks significantly associated with resistance to one or both of the two aphid biotypes studied. Finally, we identified candidate genes underlying ApRVII that are potentially involved in plant-aphid interactions and marker haplotypes linked with aphid resistance. This study sets the ground for the functional characterization of molecular pathways involved in pea defence to the aphids but also is a step forward for breeding aphid-resistant cultivars.

Differences in egg hatching time between cyclical and obligate parthenogenetic lineages of aphids.

Many aphid species exhibit a variation in reproductive mode which is influenced by winter climate regimes, with cyclical parthenogenetic (CP) lines dominating in cold winter areas (because they produce cold-resistant eggs) and obligate parthenogenetic (OP) ones in mild winter regions (because of their parthenogenetic overwintering). Genetic studies on several aphid species have shown that the OP trait can be transmitted during sexual events involving the 2 types of lines. This genetic system could be considered as a local safeguarding mechanism for OP alleles in case severe frost would have killed all parthenogenetically overwintering individuals. However, this strategy would only be efficient in restoring local polymorphism in breeding systems if the newly hatched OP recombinants remain competitive over their CP counterparts. In this study we compared egg hatching sequences of CP and OP F1 clones from several crosses obtained for 2 cereal aphid species, Sitobion avenae (constant 5 °C, 8 h of light) and Rhopalosiphum padi (winter outdoor conditions). For S. avenae, we obtained F1 offspring from 6 crosses, involving 4 clones while in R. padi F1 were obtained from 11 crosses involving 14 clones. We showed that in both species proportions of OP clones were higher in the first half of the progeny relative to the second half. In addition, F1 OP clones hatched in the mean about a week earlier than their CP sibs, which gives them a demographic advantage at the start of the growth season. We then discussed the consequences of this fitness advantage for the maintenance and spread of the OP trait in aphid populations.

Conditional Reduction of Predation Risk Associated with a Facultative Symbiont in an Insect.

Symbionts are widespread among eukaryotes and their impacts on the ecology and evolution of their hosts are meaningful. Most insects harbour obligate and facultative symbiotic bacteria that can influence their phenotype. In the pea aphid Acyrthosiphon pisum, an astounding symbiotic-mediated phenotype has been recently observed: when infected with the symbiotic bacteria Rickettsiella viridis, young red aphid larvae become greener at adulthood and even darker green when co-infected with Rickettsiella viridis and Hamiltonella defensa. As body colour affects the susceptibility towards natural enemies in aphids, the influence of the colour change due to these facultative symbionts on the host survival in presence of predators was tested. Our results suggested that the Rickettsiella viridis infection may impact positively host survival by reducing predation risk. Due to results from uninfected aphids (i.e., more green ones attacked), the main assumption is that this symbiotic infection would deter the predatory ladybird feeding by reducing the profitability of their hosts rather than decreasing host detection through body colour change. Aphids co-infected with Rickettsiella viridis and Hamiltonella defensa were, however, more exposed to predation suggesting an ecological cost associated with multiple infections. The underlying mechanisms and ecological consequences of these symbiotic effects are discussed.

Facultative symbiont infections affect aphid reproduction.

Some bacterial symbionts alter their hosts reproduction through various mechanisms that enhance their transmission in the host population. In addition to its obligatory symbiont Buchnera aphidicola, the pea aphid Acyrthosiphon pisum harbors several facultative symbionts influencing several aspects of host ecology. Aphids reproduce by cyclical parthenogenesis whereby clonal and sexual reproduction alternate within the annual life cycle. Many species, including the pea aphid, also show variation in their reproductive mode at the population level, with some lineages reproducing by cyclical parthenogenesis and others by permanent parthenogenesis. While the role of facultative symbionts has been well studied during the parthenogenetic phase of their aphid hosts, very little is known on their possible influence during the sexual phase. Here we investigated whether facultative symbionts modulate the capacity to produce sexual forms in various genetic backgrounds of the pea aphid with controlled symbiont composition and also in different aphid genotypes from natural populations with previously characterized infection status and reproductive mode. We found that most facultative symbionts exhibited detrimental effects on their hosts fitness under sex-inducing conditions in comparison with the reference lines. We also showed that the loss of sexual phase in permanently parthenogenetic lineages of A. pisum was not explained by facultative symbionts. Finally, we demonstrated that Spiroplasma infection annihilated the production of males in the host progeny by inducing a male-killing phenotype, an unexpected result for organisms such as aphids that reproduce primarily through clonal reproduction.

Effect of host defense chemicals on clonal distribution and performance of different genotypes of the cereal aphid Sitobion avenae.

Five microsatellite loci were used to study the genetic variability and population structure of Sitobion avenae (Hemiptera: Aphididae) on some of its host plants. Individuals were collected in Chile from different cultivated and wild Poaceae. Forty-four multilocus genotypes were found among the 1052 aphids analyzed, of which four represented nearly 90% of the sample. No specialist genotypes were found, although some preferred hosts endowed with chemical defenses, i.e., hydroxamic acids (Hx), while others preferred comparatively undefended hosts. Performances of some predominant and some rare genotypes were evaluated on plants differing in their Hx levels. Significant differences in performance were found among clones, the two most common genotypes showing no differences in performance among all hosts tested, and the rare genotypes showing enhanced performance on the host with highest Hx level. A hypothesis is proposed whereby the appearance of rarer genotypes is in part related to the presence of Hx.

Lack of detectable genetic recombination on the X chromosome during the parthenogenetic production of female and male aphids.

We used polymorphic microsatellite markers to look for recombination during parthenogenetic oogenesis between the X chromosomes of aphids of the tribe Macrosiphini. We examined the X chromosome because it comprises approximately 25 % of the genome and previous cytological observations of chromosome pairing and nucleolar organizer (NOR) heteromorphism suggest recombination, although the same is not true for autosomes. A total of 564 parthenogenetic females of Myzus clones with three distinct reproductive modes (cyclical parthenogenesis, obligate parthenogenesis and obligate parthenogenesis with male production) were genotyped at three informative X-linked loci. Also, parthenogenetically produced males from clones encompassing the full range of male-producing reproductive strategies were genotyped. These included 391 Myzus persicae males that were genotyped at three X-linked loci and 538 males from Sitobion clones that were genotyped at five informative X-linked loci. Our results show no departure from clonality in parthenogenetic generations of aphids of the tribe Macrosiphini: no recombinant genotypes were observed in parthenogenetically produced males or females.

Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae.

Aphids typically reproduce by cyclical parthenogenesis, with a single sexual generation alternating with numerous asexual generations each year. However, some species exhibit different life cycle variants with various degrees of investment in sexuality. We tested the hypothesis that these life cycle variants are selected in space and time by climatic factors, mainly winter severity, due to an ecological link between sexual reproduction and the production of a cold-resistant form, the egg. More than 600 clones of the aphid Sitobion avenae F. were collected in five to six regions of France with contrasting climates during 3 consecutive years and compared for their production of sexual forms in standardised conditions. As predicted by a recent model of breeding system distribution and maintenance in aphids, we found a clear shift between northern and southern populations, with decreasing sexuality southwards. Life cycle variants investing entirely or partly in sexual reproduction in autumn predominated in northern sites, while obligate parthenogens and male-producers dominated in the southern sites. No clear east-west pattern of decreasing sexuality was found, and annualvariation in the relative proportions of life cycle variants was not clearly influenced by the severity of the previous winter. These latter results suggest that other selection pressures could interact with winter climate to determine the local life cycle polymorphism in S. avenae populations.