Not only is ecological specialization a defining feature of much of Earth's biological diversity, the evolution of specialization may also play a central role in generating diversity by facilitating speciation. To understand how ecological specialization evolves, we must know the particular characters that cause organisms to be specialized. For example, most theories of specialization in herbivorous insects emphasize physiological trade-offs in response to toxic plant chemicals. However, even in herbivores, it is likely that other characters are also involved in resource specialization. Knowing the causes of ecological specialization is also crucial for linking specialization to speciation. When the same character(s) that cause specialization also influence assortative mating, speciation may occur particularly rapidly because specialization and reproductive isolation become coupled in a positive feedback that speeds the evolution of both. Indeed, a central hypothesis in the study of ecological speciation is that specialization in recently diverged taxa may often be due to characters that also produce assortative mating. We test this hypothesis by evaluating the causes of ecological specialization among host-associated populations of an herbivorous insect, the pea aphid (Acyrthosiphon pisum). These populations are highly specialized on different host plants (alfalfa or clover; "alternate hosts"), and the races are partially reproductively isolated. Here, we identify key characters responsible for host plant specialization. Our results suggest that the major proximal determinant of host specialization is the behavioral acceptance of a plant rather than the toxicity of the food source. Pea aphids rapidly assess alfalfa and clover and reject the alternate host based on chemical cues that are perceived before the initiation of feeding. This rapid behavioral rejection of the alternate host by a given race has two consequences. First, unrestrained aphids quickly leave the alternate host and search for other plants. Because pea aphids mate on their host plants, divergence in host acceptance among ecologically specialized races leads to congregation on the favored host. This results in de facto assortative mating when sexual forms are produced in late summer. Second, specialized aphids that are held on the alternate host will not feed in a 7.2-h trial, even in the face of starvation. Thus, a complex trait, behavioral acceptance of a plant as host, influences both reproductive isolation (through host-associated assortative mating) and ecological specialization (because of low nutritional uptake on the alternate host). This dual influence of feeding behavior on both assortative mating and resource specialization is central to the maintenance of these divergent races, and it may also have been involved in their origin.
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.
We have initiated research to determine the genetic basis of a male wing polymorphism in the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae). Previous studies showed that this polymorphism is controlled by a single biallelic locus, which we name aphicarus (api), on the X chromosome. Our objectives were to confirm that api segregates as a polymorphism of a single gene on the X chromosome, and to obtain molecular markers flanking api that can be used as a starting point for high-resolution genetic and physical mapping of the target region, which will ultimately allow the cloning of api. We have established an F 2 population segregating for api and have generated X-linked AFLP markers. The segregation pattern of api in the F 2 population shows that the male wing polymorphism segregates as a polymorphism of a single gene, or set of closely linked genes on the X chromosome. Using a subset of 78 F 2 males, we have constructed a linkage map of the chromosomal region encompassing api using seven AFLP markers. The map spans 74.1 cM and we have mapped api to an interval of 10 cM. In addition, we confirmed X linkage of our AFLP markers and api by using one X-linked marker developed in an earlier study. Our study presents the first mapping of a gene with known function in aphids, and the results indicate that target gene mapping in aphids is feasible. Heredity (2005) 94, 435-442.
Sexual forms of two genotypes of the aphid Schizaphis graminum, one a vector, the other a nonvector of two viruses that cause barley yellow dwarf disease (Barley yellow dwarf virus [BYDV]-SGV, luteovirus and Cereal yellow dwarf virus-RPV, polerovirus), were mated to generate F1 and F2 populations. Segregation of the transmission phenotype for both viruses in the F1 and F2 populations indicated that the transmission phenotype is under genetic control and that the parents are heterozygous for genes involved in transmission. The ability to transmit both viruses was correlated within the F1 and F2 populations, suggesting that a major gene or linked genes regulate the transmission. However, individual hybrid genotypes differed significantly in their ability to transmit each virus, indicating that in addition to a major gene, minor genes can affect the transmission of each virus independently. Gut and salivary gland associated transmission barriers were identified in the nonvector parent and some progeny, while other progeny possessed only a gut barrier or a salivary gland barrier. Hemolymph factors do not appear to be involved in determining the transmission phenotype. These results provide direct evidence that aphid transmission of luteoviruses is genetically regulated in the insect and that the tissue-specific barriers to virus transmission are not genetically linked.
Many polyphenisms are examples of adaptive phenotypic plasticity where a single genotype produces distinct phenotypes in response to environmental cues. Such alternative phenotypes occur as winged and wingless parthenogenetic females in the pea aphid (Acyrthosiphon pisum). However, the proportion of winged females produced in response to a given environmental cue varies between clonal genotypes. Winged and wingless phenotypes also occur in males of the sexual generation. In contrast to parthenogenetic females, wing production in males is environmentally insensitive and controlled by the sex-linked, biallelic locus, aphicarus (api ). Hence, environmental or genetic cues induce development of winged and wingless phenotypes at different stages of the pea aphid life cycle. We have tested whether allelic variation at the api locus explains genetic variation in the propensity to produce winged females. We assayed clones from an F 2 cross that were heterozygous or homozygous for alternative api alleles for their propensity to produce winged offspring. We found that clones with different api genotypes differed in their propensity to produce winged offspring. The results indicate genetic linkage of factors controlling the female wing polyphenism and male wing polymorphism. This finding is consistent with the hypothesis that genotype by environment interaction at the api locus explains genetic variation in the environmentally cued wing polyphenism.
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