Evolution of host specialization in the Adelgidae (Insecta: Hemiptera) inferred from molecular phylogenetics

The Adelgidae form a small group of insects in the Aphidoidea. They are cyclically parthenogenetic with host alternating, multiple-generation complex life cycles and are restricted to certain host genera in the Pinaceae. Species that host alternate always have Picea as the primary host where sexual reproduction and gall formation occur, and another genus in the Pinaceae as the secondary host where a series of parthenogenetic generations are produced. Other species that do not host alternate complete their entire life cycle on one host and only reproduce parthenogenetically. We studied relationships within Adelgidae using DNA sequences from the mitochondrial COI, COII, and cytb genes, and the nuclear EF1alpha gene. Analysis of the combined data resulted in a well-resolved phylogeny in which the major adelgid clades correspond neatly to their association with secondary host genera. Specialization on each secondary host genus occurred only once and was followed by diversification on the host genus. Molecular dating of divergence times in the Adelgidae suggest that diversification among host genera occurred in the Late Cretaceous and Early Tertiary when the Pinaceae genera were diverging. It is not clear, however, whether the Adelgidae and Pinaceae co-diversified because the relationships among the Pinaceae genera are not fully resolved. We discuss implications for adelgid taxonomy, life cycle evolution, and evolution of the interaction between adelgids and their host plants.     

A holocyclic life cycle in a gall-forming adelgid, Adelges japonicus (Homoptera: Adelgidae)

While the family Adelgidae (Homoptera) is typically holocyclic and periodically host-alternating between a primary and secondary host, some anholocyclic species may persist exclusively on the primary or secondary host. In this study, we investigated the life cycle of Adelges japonicus , an anholocyclic species that utilizes either Picea jezoensis and Picea sitchensis (Pinaceae) as the primary hosts. Transfer experiments conducted in Hokkaido, the northern-most island of Japan, revealed that A. japonicus also includes holocyclic forms that can migrate to the secondary host, Larix kaempferi . The holocyclic forms differed from anholocyclic forms in the date of gall dehiscence, oviposition preference of gallicolae and development of wax gland plates of gallicola adults. However, we treated these two forms as the same species because of a lack of information on their phylogenetic relationships and genetic isolation. Sequence of generations and developmental stages of each generation in the holocyclic forms were reported. Morphology of wax gland plates of first-instar exulis was consistent with those of the subgenus Cholodkovskya , but different from those of the subgenus Adelges , to which A. japonicus has been assigned. Morphological comparison of gallicola adults suggests that the holocyclic forms were introduced to Hokkaido from central Japan.     

Responses of holocyclic and anholocyclic Rhopalosiphum padi populations to low‐temperature and short‐photoperiod induction

The different life cycles of aphid species make these organisms good models for studying the short‐term consequences of sex. The bird cherry‐oat aphid Rhopalosiphum padi has a wide geographic distribution and correspondingly different life cycles. In this study, the life cycles of R. padi collected from six different regions in China were characterized experimentally by comparing the responses of holocyclic and anholocyclic populations to low‐temperature and short‐photoperiod induction. Clones collected from Chuzhou, Taian, and Taigu consistently reproduced via obligate parthenogenesis, whereas clones from Hami and Baicheng were holocyclic in their response, and those from Lanzhou were both holocyclic and anholocyclic. Prolonged exposure to low temperature and a short photoperiod (LS) had negative effects on the offspring of anholocyclic aphids with regard to adult lifespan, total longevity, and fecundity compared with aphids maintained at a normal temperature and a long photoperiod (NL). Holocyclic LS R. padi had longer developmental times at all nymph stages, a shorter adult lifespan, shorter total longevity, and a lower fecundity than NL counterparts. The adult prereproduction period of gynoparae was significantly longer than that of virginoparae, and the total longevity of gynoparae was significantly shorter than that of virginoparae. Moreover, the net reproductive and gross reproduction rates, as well as the total fecundity, were roughly fivefold higher in virginoparae than in gynoparae, indicating that there is the short‐term cost of sex. When maintained on their secondary host (Triticum aestivum), gynoparae, males, and oviparae produced by holocyclic populations could survive, and gynoparae produced oviparae. However, under NL conditions, oviparae could not produce overwintering eggs on the secondary host, whereas a few overwintering eggs were generated by oviparae under LS conditions. Taken together, these results illuminate the complexity of insect responses and contribute to a complete understanding of the aphid life cycle and its evolution.     

Melatonin in the seasonal response of the aphid Acyrthosiphon pisum

Aphids display life cycles largely determined by the photoperiod.During the warm long-day seasons.most aphid species reproduce by viviparous parthenogenesis.The shortening of the photoperiod in autumn induces a switch to sexual reproduction.Males and sexual females mate to produce overwintering resistant eggs.In addition to this full life cycle(holocycle),there are anholocyelic lineages that do not respond to changes in photoperiod and reproduce continuously by parthenogenesis.The molecular or hormonal events that trigger the scasonal response(i.c,induction of the sexual phenotypes)are still unknown.Although circadian synthesis of melatonin is known to play a key role in vertebrate photoperiodism,the involvement of the circadian clock and/or of the hor-mone melatonin in insect seasonal responses is not so well established.Here we show that melatonin levels in the aphid Acyrthosiphon pisum are significantly higher in holocyclice aphids reared under short days than under long days,while no differences were found between anholoeyelic aphids under the same conditions.We also found that melatonin is localized in the aphid suboesophageal ganglion(SOG)and in the thoracic ganglionic mass(TGM).In analogy to vertcbrates,insect-type arylalkxylamine N-acetyltransferases(i-AANATs)are thought to play a key role in melatonin synthesis.We measured the expression of four I-AANAT genes identified in A.pisum and localized two of them in situ in the insect central nervous systems(CNS).Levels of expression of these genes were compatible with the quantities of melatonin observed.Moreover,like melatonin,expression of these genes was found in the SOG and the TGM.     

Taxonomic identity of a galling adelgid (Hemiptera: Adelgidae) from three spruce species in Central Japan

Gall‐forming insects are commonly highly host‐specific, and galling species once thought to be oligo‐ or polyphagous are often found to represent a complex of host‐specific races or cryptic species. A recent DNA barcoding study documented that an unidentified species of the genus Adelges is a gall‐former associated with four spruce species (Picea bicolor, P. koyamai, P. maximowiczii, P. polita) as the primary hosts, with little genetic differentiation among insects on different host species. In this study, we investigated the morphology of this galling adelgid to determine its taxonomic identity. Morphological inspection of insects collected from three of the spruce species confirmed that this adelgid is a single galling species, and is identified as Adelges (Sacchiphantes) kitamiensis, which was previously known only from the secondary host. We described the gallicola adults of this species, as well as the first‐instar exules which are the offspring of gallicolae. Finally, we verified the taxonomic identity of this species and discuss its life cycle and host distribution.     

球蚜科分类概述

球蚜科是蚜虫类的一个重要类群,包括多种林业害虫和检疫害虫,本文从形态特征、生活史、寄主植物、地理分布,进化起源等方面对世界及中国球蚜物种进行了综合论述.结果表明,球蚜科具有较多原始的特征,是蚜虫中较为古老的一类;球蚜具有包括异寄主全周期、异寄主不全周期、同寄主不全周期等复杂的生活周期,形成虫瘿是其主要的为害特征;球蚜科物种专性寄生在松科植物上,主要包括云杉属Picea、松属Pinus、落叶松属Larix、冷杉属Abies等属的植物,在蚜虫物种和寄主植物之间存在着平行演化的现象;球蚜的分布与寄主植物的分布相一致,主要是北半球温带和亚热带高山.世界球蚜有8属59种,区系成分主要是新北区、古北区.中国球蚜科有6属20种,分布在黑龙江、云南、四川等地,主要是古北区成分.初步推测球蚜科可能首先在松属植物上起源.     

Evolutionary lability of a complex life cycle in the aphid genus <Emphasis Type="Italic">Brachycaudus</Emphasis>

Background  

Most aphid species complete their life cycle on the same set of host-plant species, but some (heteroecious species) alternate between different hosts, migrating from primary (woody) to secondary (herbaceous) host plants. The evolutionary processes behind the evolution of this complex life cycle have often been debated. One widely accepted scenario is that heteroecy evolved from monoecy on woody host plants. Several shifts towards monoecy on herbaceous plants have subsequently occurred and resulted in the radiation of aphids. Host alternation would have persisted in some cases due to developmental constraints preventing aphids from shifting their entire life cycle to herbaceous hosts (which are thought to be more favourable). According to this scenario, if aphids lose their primary host during evolution they should not regain it. The genus Brachycaudus includes species with all the types of life cycle (monoecy on woody plants, heteroecy, monoecy on herbs). We used this genus to test hypotheses concerning the evolution of life cycles in aphids.     

Ancient and modern colonization of North America by hemlock woolly adelgid,Adelges tsugae (Hemiptera: Adelgidae), an invasive insect from East Asia

Hemlock woolly adelgid, Adelges tsugae, is an invasive pest of hemlock trees (Tsuga) in eastern North America. We used 14 microsatellites and mitochondrial COI sequences to assess its worldwide genetic structure and reconstruct its colonization history. The resulting information about its life cycle, biogeography and host specialization could help predict invasion by insect herbivores. We identified eight endemic lineages of hemlock adelgids in central China, western China, Ulleung Island (South Korea), western North America, and two each in Taiwan and Japan, with the Japanese lineages specializing on different Tsuga species. Adelgid life cycles varied at local and continental scales with different sexual, obligately asexual and facultatively asexual lineages. Adelgids in western North America exhibited very high microsatellite heterozygosity, which suggests ancient asexuality. The earliest lineages diverged in Asia during Pleistocene glacial periods, as estimated using approximate Bayesian computation. Colonization of western North America was estimated to have occurred prior to the last glacial period by adelgids directly ancestral to those in southern Japan, perhaps carried by birds. The modern invasion from southern Japan to eastern North America caused an extreme genetic bottleneck with just two closely related clones detected throughout the introduced range. Both colonization events to North America involved host shifts to unrelated hemlock species. These results suggest that genetic diversity, host specialization and host phylogeny are not predictive of adelgid invasion. Monitoring non‐native sentinel host trees and focusing on invasion pathways might be more effective methods of preventing invasion than making predictions using species traits or evolutionary history.     

Genetic variation in natural populations of the aphid Rhopalosiphum padi as revealed by maternally inherited markers

A survey on 148 clones of the aphid Rhopalosiphum padi from 11 widespread localities has been carried out to study the genetic structure of populations of this species as revealed by mitochondrial DNA restriction site and length polymorphisms as well as by restriction site analysis of a maternally inherited plasmid carried by the aphid eubacterial endosymbiont Buchnera aphidicola. Our results support the existence in the area under study of two main aphid maternal lineages strikingly coincidental with the two main reproductive categories displayed by this species. Those aphid clones possessing an incomplete life cycle that lacks the sexual phase (anholocyclic or androcyclic clones) show mitochondrial DNA (mtDNA) haplotype I and plasmid haplotype I, whereas those clones displaying the complete life cycle (holocyclic clones) posses some other distinct mtDNA haplotypes closely related to each other and plasmid haplotype II. While restriction-site analysis of maternally inherited markers points to a relatively ancient origin of anholocycly/androcycly (between 460 000 and 1 400 000 years) followed by interrupted gene flow with respect to the ancestral holocyclic population, mtDNA size variation also suggests that historical stochastic processes have a different effect on the evolution of both main aphid lineages. Evidence of occasional nuclear gene flow between lineages and its consequences on the correspondence between maternally inherited haplotypes and life cycle are also presented and discussed.     

Effect of reproductive mode on host plant utilization of melon aphid (Hemiptera: Aphididae)

Variation in the reproductive mode of melon aphid Aphis gossypii Glover occurred on the large geographic scale, but the performance of different reproductive modes to use host plant is poorly understood. Life tables of melon aphid population that undergo the anholocyclic, androcyclic, and intermediate reproductive mode were conducted on different host plants. The results showed that the anholocyclic and androcyclic strains could become adults and produce offspring on cotton Gossypium hirsutum L., whereas the intermediate strain could not. The survival rate, net reproductive rate (R(0)), and intrinsic rate of natural increase (r(m)) of the androcyclic strain on cotton were significantly greater than that of the anholocyclic strain. The three strains could aptly use cucurbits host plants including cucumber Cucumis sativa L., pumpkin Cucurbita moschata (Duchesne ex Lam.), and zucchini Cucurbita pepo L.; survival rate and R(0) were not significantly different on these two host plants. Moreover, the r(m) of the anholocyclic strain on cucumber and the androcyclic strain on pumpkin and zucchini were significantly greater than that of the other two strains. The abilities of the three strains to use a host plant were flexible, because their r(m) on pumpkin or zucchini became equal after rearing for four successive generations; furthermore, the intermediate strain attained the ability to use cotton, and the performance of anholocyclic and intermediate strains to use cotton also significantly increased after feeding on pumpkin or zucchini for one or three generations. It was concluded that the reproductive mode and feeding experience affected the performance of melon aphid to use a host plant.     

First record of Adelges (Cholodkovskya) viridanus (Hemiptera: Adelgidae) in North America,with a description of the fundatrix form in Japan

Adelges (Cholodkovskya) viridanus (Cholodkovsky 1896) (Hemiptera: Adelgidae) is found throughout Eurasia where it is understood to be anholocyclic, feeding on species of larch (Larix), without host alternation. For the first time, we report this species in North America, outside of its native range, from specimens collected in an arboretum in Ohio, USA. Molecular phylogenetic analysis was inconclusive as to whether it was introduced from Europe or Asia. In addition, specimens collected from Picea jezoensis in Japan were confirmed for the first time as A. (C.) viridanus by matching DNA sequences to specimens collected on Larix. Therefore, A. (C.) viridanus is either capable of completing a host-alternating holocycle in Japan, or includes very recently diverged anholocyclic populations on Picea. Finally, we describe the adult fundatrix form, which was previously unknown.     

Life cycle variation of Myzus persicae (Hemiptera: Aphididae) in Greece

During the years 1995-1999 the life cycle category of 2797 clones of Myzus persicae (Sulzer) was examined. The clones originated from primary and secondary hosts from different localities of North and Central Greece and the island of Crete in the south. Four different overwintering life cycle strategies were found that have also been described for M. persicae and other heteroecious species previously. A geographical variation was found in the proportion of holocyclic clones from tobacco and other secondary hosts associated with the abundance of the primary host in the sampling regions. In Central Macedonia, around the main peach-growing regions, the proportion of holocyclic clones was mostly above 50% and in some cases reached 100%. In localities of East Macedonia, holocyclic clones were also frequent. On the other hand, further south or in north-eastern Greece, where peach is not common, the proportion of holocyclic clones varied between 0 and 33%. Fifty seven percent of examined anholocyclic clones produced males under short day conditions, suggesting that androcyclic clones in Greece represent an important factor of genetic variability. Intermediate clones were sampled from all host-plants but at low frequencies (3.6% of total examined clones and 6.9% of non-holocyclic ones). Moreover, a regional variation was found in different colour forms feeding on tobacco plants. Red clones were predominant in regions where aphids overwinter parthenogenetically on weeds or winter crops. However, almost all clones from the primary host were green. The ecological aspects of life cycle variation are discussed.     

Complex life cycles drive community assembly through immigration and adaptive diversification

Most animals undergo ontogenetic niche shifts during their life. Yet, standard ecological theory builds on models that ignore this complexity. Here, we study how complex life cycles, where juvenile and adult individuals each feed on different sets of resources, affect community richness. Two different modes of community assembly are considered: gradual adaptive evolution and immigration of new species with randomly selected phenotypes. We find that under gradual evolution complex life cycles can lead to both higher and lower species richness when compared to a model of species with simple life cycles that lack an ontogenetic niche shift. Thus, complex life cycles do not per se increase the scope for gradual adaptive diversification. However, complex life cycles can lead to significantly higher species richness when communities are assembled trough immigration, as immigrants can occupy isolated peaks of the dynamic fitness landscape that are not accessible via gradual evolution.     

Morphogenetic bases and parametric system of trichome evolution in plants of the genus <Emphasis Type="Italic">Draba</Emphasis> L.

Using quantitative morphological analysis of light microscopy data, the normal variation of trichome morphogenesis is studied in six whitlow grass species (Draba L.) and the morphological variation of adult trichomes in 11 species. The evolution consists in the transition from a radial morphogenesis pattern to bilateral and replacement of complex (branched) trichome rays with simple (unbranched) rays. A parametric system is constructed for classification of the ray morphology; this system includes two parameters—the ratio of the numbers of complex to simple rays, characterizing the probability of secondary branching of primary buds, and the number of primary buds, characterizing the probability of primary branching on the surface of the trichome cell. In this parametric space, all of the studied species fit well a third-order curve consisting of two ascending branches displaying a positive correlation between the primary and secondary branchings and a descending branch, located between them, where the primary and secondary branches are negatively correlated. The deduced evolutionary direction is almost independent of the size of the trichome cells and is explained exclusively by the mechanics of morphogenesis: acceleration in the development of the primary bud of the ray decreases the probability of its own branching and creates additional elastic extension of the cell surface, preventing other buds from branching. The morphogenesis itself appears to be a mechanically nonholonomic system, filtering in a selective manner the fluctuations of the same sign, which explains the directed pattern of its evolution. In the evolutionarily initial state, trichome ontogenesis is absent because its modules (primary buds) are formed by a mirror duplication. The ontogenesis commences when mirror symmetry in the formation of modules is lost and replaced with an axial pattern; thus, the change in the morphological type of buds is a direct consequence of the emergence of ontogenesis and its further evolution. Its main material is intraindividual variation, the only source of which is the mechanics of morphogenesis itself. It is found that morphological evolution can take place at an initially zero heritability and zero adaptive value of morphological differences.     

DEMOGRAPHIC MECHANISMS DETERMINING THE DYNAMICS OF THE RELATIVE ABUNDANCE OF PHASES IN BIPHASIC LIFE CYCLES1

Studies investigating the demographic traits that drive the patterns of phase dominance (the ploidy ratio) in isomorphic biphasic life cycles have not found an integrative solution. Either fertility or survival has been suggested independently as the main driver. Here, we provide a global theoretical framework on how demographic mechanisms determine the ploidy ratio, unifying previous numerical and observational attempts at this question. The analytical solutions of both the ploidy ratio and its elasticities to model parameters of a stage/size‐structured model patterned after the life cycle of a marine alga were derived and analyzed. A complex interaction among vital rates determines the patterns of phase dominance of biphasic life cycles. Three co‐occurring processes—growth, fertility, and looping—may dominate the dynamics of the population, determining both its growth rate and ploidy ratio. Our analyses show that in species where fertility is low, the ploidy ratio is highly elastic to looping transitions (survival, breakage, and clonal growth). Consequently, the subtle morphological, ecophysiological, and biochemistry phase differences that have been reported in isomorphic life cycles as not explaining the observed ploidy ratios, may, in fact, explain them if they translate into slight phase differences in looping transitions. In species where fertility is low, the looping dissimilarities between phases cannot be too high favoring simultaneously one phase, as the population structure would be completely dominated by that phase. In the case of ecological similarity between phases (equal looping and growth rates between phases), a ploidy ratio different from one can only be set by strong phase differences in fertility.     

Defensive Behavior in Primary- and Secondary-Host Generations of the Soldier-Producing Aphid, Pemphigus bursarius (Hemiptera: Aphididae)

The genus Pemphigus comprises several species that produce soldiers (defensive morphs) in galls on the primary host. At the moment, it is unclear if host-alternating species also produce defenders on their secondary host. We therefore examined how P. bursarius morphs of the secondary host generations respond to predators to test whether they show defensive behavior. We further examined how this response compares with the antipredator behavior of soldiers in P. bursarius and P. spyrothecae occurring on the primary host. We performed two manipulative experiments using two predatory species to quantify the behavior of the different morphs in response to predators. In both experiments, secondary host morphs of P. bursarius showed no attacking behavior and antipredator behavior in these morphs was limited to escaping natural enemies by walking away. In contrast, the first instars of the primary host generations in both Pemphigus species showed attacking behavior and were capable of killing the predators.     

我国烟蚜种群分化的RAPD分析

用RAPD-PCR技术研究了我国烟草上烟蚜Myzus persicae (Sulzer)的种群分化。结果表明：我国烟蚜的不同地理种群和不同体色之间DNA均呈现出多态性,且不同的引物可在不同水平上反应出烟蚜种群的DNA多态性。Nei的遗传距离表明我国烟草上烟蚜的分化仅在种群水平上,并未达到亚种水平。用相似性指数和Nei的遗传距离对所筛选的三个引物OPX-04、OPX-06和OPX-19的扩增结果进行聚类,虽然二者的结果不一致,但均可反应出烟蚜的地理种群和体色生物型的DNA差异。在DNA水平上,与完全周期生活史的烟蚜相比,完全周期和不完全周期生活史混合发生的烟蚜与不完全周期生活史的烟蚜更为接近,而两种生活史混合发生的烟蚜之间无明显差异。从体色看,红色比黄绿色更接近褐色。     

Variability in the developmental parameters of bird cherry–oat aphid <Emphasis Type="Italic">Rhopalosiphum padi</Emphasis> (L.) (Homoptera,Aphididae) clones during the life cycle as a genotypic adaptation

The complexity of life cycles, clonal structure of populations, and polymorphism underpin the ability of aphids to quickly evolve adaptations and inflict greater damage to crops. Harmfulness of aphids can only be limited by controlling changes in the adaptive norm that occur during seasonal cycles. In this study, timing of emergence of the main morphs and their developmental traits as reflected in 27 parameters are established for 9 heteroecious holocyclic clones of the bird cherry–oat aphid Rhopalosiphum padi (Linnaeus, 1758). On the basis of ranking the clones by the performance index, 3 clones with good performance and 4 clones with bad performance were identified. Three intermediate clones were discovered, which are capable of prolonged anholocyclic development and of overwintering at the active stage. Omission of the generation that develops on the primary host may change the population dynamics and harmfulness of aphids on secondary hosts. It is shown that performance of clones should be assessed by using demographic characteristics of morph development and phenological and behavioral peculiarities. The work was carried out under field conditions and in outdoor metal grid cages.