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Abstract Many plant-sap-feeding insects have maintained a single, obligate, nutritional symbiont over the long history of their lineage. This senior symbiont may be joined by one or more junior symbionts that compensate for gaps in function incurred through genome-degradative forces. Adelgids are sap-sucking insects that feed solely on conifer trees and follow complex life cycles in which the diet fluctuates in nutrient levels. Adelgids are unusual in that both senior and junior symbionts appear to have been replaced repeatedly over their evolutionary history. Genomes can provide clues to understanding symbiont replacements, but only the dual symbionts of hemlock adelgids have been examined thus far. Here, we sequence and compare genomes of four additional dual-symbiont pairs in adelgids. We show that these symbionts are nutritional partners originating from diverse bacterial lineages and exhibiting wide variation in general genome characteristics. Although dual symbionts cooperate to produce nutrients, the balance of contributions varies widely across pairs, and total genome contents reflect a range of ages and degrees of degradation. Most symbionts appear to be in transitional states of genome reduction. Our findings support a hypothesis of periodic symbiont turnover driven by fluctuating selection for nutritional provisioning related to gains and losses of complex life cycles in their hosts.more » « less
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Abstract TheAdelges(Dreyfusia)piceae(Ratzeburg) species complex is a taxonomically unstable group of six species. Three of the species are cyclically parthenogenetic [Ad.nordmannianae(Eckstein),Ad.prelli(Grossmann), andAd.merkeri(Eichhorn)] and three are obligately asexual [Ad.piceae,Ad.schneideri(Börner), andAd.nebrodensis(Binazzi & Covassi)]. Some species are high‐impact pests of fir (Abies) trees, so stable species names are needed to communicate effectively about management. Therefore, to refine species delimitation, guided by a reconstruction of their biogeographic history, we genotyped adelgids from Europe, North America, and the Caucasus Mountains region with 19 microsatellite loci, sequenced the COI DNA barcoding region, and compared morphology. Discriminant analysis of principal components of microsatellite genotypes revealed four distinct genetic clusters. Two clusters were morphologically consistent withAd.nordmannianae. One of these clusters consisted of samples from the Caucasus Mountains and northern Turkey, and the other included samples from this region as well as from Europe and North America, whereAd.nordmannianaeis invasive. A third cluster was morphologically consistent withAd.piceae, and included individuals from Europe, where it is native, and North America, where it is invasive. In North America, the majority ofAd.piceaeindividuals were assigned to two geographically widespread clones, suggesting multiple introductions. The fourth cluster included individuals morphologically consistent withAd.prelliorAd.merkeri. However, based on genetic assignments, hybrid simulations, and approximate Bayesian computation, we find it likely that these are contemporary hybrids betweenAd.nordmannianaeandAd.piceaethat arose independently in Europe and North America, so we propose thatAd.prelliandAd.merkeriare invalid. Finally, we synonymiseAd.schneideri(syn.n.)withAd.nordmannianaeand designateAd.nebrodensisas subspeciesAd.piceae nebrodensis(stat.n.). Our revised taxonomy therefore recognises two species:Ad.nordmannianaeandAd.piceae, which we estimate to have diverged recently, during one of the last two interglacial periods. Finally, we comment on this species complex being in the midst of transition between sexual and asexual reproduction, a pattern that is probably common in Adelgidae.more » « less
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