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Intrinsic pre-zygotic reproductive isolation of distantly related pea aphid host races.

ABSTRACT: Human activities may weaken or destroy reproductive isolation between young taxa, leading to their fusion with consequences for population and community ecology. Pea aphid host races are adapted to different legume taxa, providing a degree of pre-mating isolation mediated by habitat choice. Yet, all races can feed and reproduce on the broad bean (Vicia faba), a major crop which represents a 'universal host plant', which can promote hybridization between races. Here, we ask if pea aphid host races have reproductive barriers which prevent or reduce gene flow when they co-occur on the universal host plant. We observed mating behaviour, female survival, number of eggs and egg fertilization rates for three types of crosses: among individuals of the same host race, between closely related host races and between distantly related host races. We did not find significant differences in mating behaviour and female survival among the three types of crosses. However, we observed a drastic reduction in the number of eggs laid, and in the number of fertilized eggs, in distant crosses. We conclude that widespread broad bean cultivation in agriculture may predispose closely related-but not distantly related-host races to hybridize, disrupting reproductive isolation between incipient species.

SUBMITTER: Fazalova V

PROVIDER: S-EPMC6283932 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Intrinsic pre-zygotic reproductive isolation of distantly related pea aphid host races.

Fazalova Varvara V Nevado Bruno B McLean Ailsa A Godfray H Charles J HCJ

Biology letters 20181128 11

Human activities may weaken or destroy reproductive isolation between young taxa, leading to their fusion with consequences for population and community ecology. Pea aphid host races are adapted to different legume taxa, providing a degree of pre-mating isolation mediated by habitat choice. Yet, all races can feed and reproduce on the broad bean (<i>Vicia faba</i>), a major crop which represents a 'universal host plant', which can promote hybridization between races. Here, we ask if pea aphid ho ...[more]

PMID: 30487255

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Project description:The pea aphid (Acyrthosiphon pisum), a phloem-sucking insect, has undergone a rapid radiation together with the domestication and anthropogenic range expansion of several of its legume host plants. This insect species is a complex of at least 15 genetically different host races that can all develop on the universal host plant Vicia faba. However, each host race is specialized on a particular plant species, such as Medicago sativa, Trifolium pratense, or Pisum sativum, which makes it an attractive model insect to study ecological speciation. Previous work revealed that pea aphid host plants produce a specific phytohormone profile depending on the host plant - host race combination. Native aphid races induce lower defense hormone levels in their host plant than non-native pea aphid races. Whether these changes in hormone levels also lead to changes in other metabolites is still unknown. We used a mass spectrometry-based untargeted metabolomic approach to identify plant chemical compounds that vary among different host plant-host race combinations and might therefore, be involved in pea aphid host race specialization. We found significant differences among the metabolic fingerprints of the four legume species studied prior to aphid infestation, which correlated with aphid performance. After infestation, the metabolic profiles of M. sativa and T. pratense plants infested with their respective native aphid host race were consistently different from profiles after infestation with non-native host races and from uninfested control plants. The metabolic profiles of P. sativum plants infested with their native aphid host race were also different from plants infested with non-native host races, but not different from uninfested control plants. The compounds responsible for these differences were putatively identified as flavonoids, saponins, non-proteinogenic amino acids and peptides among others. As members of these compound classes are known for their activity against insects and aphids in particular, they may be responsible for the differential performance of host races on native vs. non-native host plants. We conclude that the untargeted metabolomic approach is suitable to identify candidate compounds involved in the specificity of pea aphid - host plant interactions.

Project description:Background and aimsThe Arctic tundra, with its extreme temperatures and short growing season, is evolutionarily young and harbours one of the most species-poor floras on Earth. Arctic species often show little phenotypic and genetic divergence across circumpolar ranges. However, strong intraspecific post-zygotic reproductive isolation (RI) in terms of hybrid sterility has frequently evolved within selfing Arctic species of the genus Draba. Here we assess whether incipient biological species are common in the Arctic flora.MethodsWe conducted an extensive crossing experiment including six species representing four phylogenetically distant families collected across the circumpolar Arctic. We crossed conspecific parental populations representing different spatial scales, raised 740 F1 hybrids to maturity and measured fertility under laboratory conditions. We examined genetic divergence between populations for two of these species (Cardamine bellidifolia and Ranunculus pygmaeus).Key resultsIn five of the six species, we find extensive reduction in pollen fertility and seed set in F1 hybrids; 219 (46 %) of the 477 F1 hybrids generated between parents separated by ≥427 km had <20 % pollen fertility. Isolation with migration (IM) and *BEAST analyses of sequences of eight nuclear genes in C. bellidifolia suggests that reproductively isolated populations of this species diverged during, or even after, the last glaciation. Likewise, Arctic populations of R. pygmaeus were genetically very similar despite exhibiting strongly reduced fertility in crosses, suggesting that RI evolved recently also in this species.ConclusionWe show that post-zygotic RI has developed multiple times within taxonomically recognized Arctic species belonging to several distantly related lineages, and that RI may have developed over just a few millennia. Rapid and widespread evolution of incipient biological species in the Arctic flora might be associated with frequent bottlenecks due to glacial cycles, and/or selfing mating systems, which are common in the harsh Arctic environment where pollinators are scarce.

Dataset Information

Intrinsic pre-zygotic reproductive isolation of distantly related pea aphid host races.

Publications

Intrinsic pre-zygotic reproductive isolation of distantly related pea aphid host races.

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