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      Aphid specialism as an example of ecological-evolutionary divergence : Aphid specialism

      1 , 2
      Biological Reviews
      Wiley

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          Abstract

          Debate still continues around the definition of generalism and specialism in nature. To some, generalism is equated solely with polyphagy, but this cannot be readily divorced from other essential biological factors, such as morphology, behaviour, genetics, biochemistry, chemistry and ecology, including chemical ecology. Viewed in this light, and accepting that when living organisms evolve to fill new ecological-evolutionary niches, this is the primal act of specialisation, then perhaps all living organisms are specialist in the broadest sense. To illustrate the levels of specialisation that may be found in a group of animals, we here provide an overview of those displayed by a subfamily of hemipteran insects, the Aphididae, which comprises some 1600 species/subspecies in Europe alone and whose members are specialised in a variety of lifestyle traits. These include life cycle, host adaptation, dispersal and migration, associations with bacterial symbionts (in turn related to host adaptation and resistance to hymenopterous wasp parasitoids), mutualisms with ants, and resistance to insecticides. As with polyphagy, these traits cannot easily be separated from one another, but rather, are interconnected, often highly so, which makes the Aphididae a fascinating animal group to study, providing an informative, perhaps unique, model to illustrate the complexities of defining generalism versus specialism.

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          Most cited references157

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          The Ants

          From the Arctic to South Africa - one finds them everywhere: Ants. Making up nearly 15% of the entire terrestrial animal biomass, ants are impressive not only in quantitative terms, they also fascinate by their highly organized and complex social system. Their caste system, the division of labor, the origin of altruistic behavior and the complex forms of chemical communication makes them the most interesting group of social organisms and the main subject for sociobiologists. Not least is their ecological importance: Ants are the premier soil turners, channelers of energy and dominatrices of the insect fauna. TOC:The importance of ants.- Classification and origins.- The colony life cycle.- Altruism and the origin of the worker caste.- Colony odor and kin recognition.- Queen numbers and domination.- Communication.- Caste and division of labor.- Social homeostasis and flexibility.- Foraging and territorial strategies.- The organization of species communities.- Symbioses among ant species.- Symbioses with other animals.- Interaction with plants.- The specialized predators.- The army ants.- The fungus growers.- The harvesters.- The weaver ants.- Collecting and culturing ants.- Glossary.- Bibliography.- Index.
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            Facultative bacterial symbionts in aphids confer resistance to parasitic wasps.

            Symbiotic relationships between animals and microorganisms are common in nature, yet the factors controlling the abundance and distributions of symbionts are mostly unknown. Aphids have an obligate association with the bacterium Buchnera aphidicola (the primary symbiont) that has been shown to contribute directly to aphid fitness. In addition, aphids sometimes harbor other vertically transmitted bacteria (secondary symbionts), for which few benefits of infection have been previously documented. We carried out experiments to determine the consequences of these facultative symbioses in Acyrthosiphon pisum (the pea aphid) for vulnerability of the aphid host to a hymenopteran parasitoid, Aphidius ervi, a major natural enemy in field populations. Our results show that, in a controlled genetic background, infection confers resistance to parasitoid attack by causing high mortality of developing parasitoid larvae. Compared with uninfected controls, experimentally infected aphids were as likely to be attacked by ovipositing parasitoids but less likely to support parasitoid development. This strong interaction between a symbiotic bacterium and a host natural enemy provides a mechanism for the persistence and spread of symbiotic bacteria.
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              Variation in resistance to parasitism in aphids is due to symbionts not host genotype.

              Natural enemies are important ecological and evolutionary forces, and heritable variation in resistance to enemies is a prerequisite for adaptive responses of populations. Such variation in resistance has been previously documented for pea aphids (Acyrthosiphon pisum) attacked by the parasitoid wasp Aphidius ervi. Although the variation was presumed to reflect genotypic differences among the aphids, another potential source of resistance to A. ervi is infection by the facultative bacterial symbiont Hamiltonella defensa. Here, we explored whether variation among symbiont isolates underlies variation among A. pisum clones in resistance to A. ervi. Although maternally transmitted, H. defensa is sometimes horizontally transferred in nature and can be experimentally established in clonal aphid lineages. We established five H. defensa isolates in a common A. pisum genetic background. All of the five isolates tested, including one originating from another aphid species, conferred resistance. Furthermore, isolates varied in levels of resistance conferred, ranging from 19% to nearly 100% resistance. In contrast, a single H. defensa isolate established in five different aphid clones conferred similar levels of resistance; that is, host genotype did not influence resistance level. These results indicate that symbiont-mediated resistance to parasitism is a general phenomenon in A. pisum and that, at least for the isolates and genotypes considered, it is the symbiont isolate that determines the level of resistance, not aphid genotype or any interaction between isolate and genotype. Thus, acquisition of a heritable symbiont appears to be a major mode of adaptation to natural enemy pressure in these insects.
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                Author and article information

                Journal
                Biological Reviews
                Biol Rev
                Wiley
                14647931
                February 2018
                February 2018
                August 23 2017
                : 93
                : 1
                : 642-657
                Affiliations
                [1 ]School of Biosciences; Cardiff University; Cardiff CF10 3AX U.K.
                [2 ]Faculty of Technical and Human Science, Department of Horticulture; Sapientia Hungarian University of Transylvania; 540485 Tirgu-Mures Romania
                Article
                10.1111/brv.12361
                28836372
                5de23db8-39db-42f0-af95-9ae657066b94
                © 2017

                http://doi.wiley.com/10.1002/tdm_license_1.1

                http://onlinelibrary.wiley.com/termsAndConditions#vor

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