Article

Population genetics of Tuberolachnus salignus, an obligate parthenogenetic aphid

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Abstract

1 This study reports the results obtained in an investigation of the putatively parthenogenetic aphid species Tuberolachnus salignus Gmelin. Tuberolachnus salignus is one of the largest aphid species in the world but where and how it overwinters is not known. It has recently become noteworthy because it is increasingly found on commercially grown willows used in bioenergy production. 2 Seven newly‐developed polymorphic microsatellite markers were used to investigate the genetic diversity of the species, and also to confirm its reproduction strategy. 3 Tuberolachnus salignus shows very low clonal diversity; only 16 genotypes were found in 660 specimens from 27 populations in five countries. 4 There was limited geographical structuring in the samples, although the two most common genotypes, which comprised more than half of the specimens collected, had a very wide distribution. 5 Furthermore, we determined that these aphids, which live in very dense colonies, can consist of more than one genotype, suggesting aggregation of colonizing T. salignus. These results confirm the parthenogenetic nature of T. salignus and demonstrate the presence of common genotypes that are widespread in time and space.

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... Genetic diversity within the species has been shown to be very low in Europe and North America (both assumed to be part of the invasive range). Aradottir et al. (2012) found only 16 genotypes amongst 660 specimens from 27 populations in five countries. The two most common genotypes comprised more than half of the specimens collected and were widely distributed, indicating strong dispersal capabilities. ...
... The two most common genotypes comprised more than half of the specimens collected and were widely distributed, indicating strong dispersal capabilities. Dense colonies of T. salignus can consist of more than one genotype, possibly because of aggregation by dispersing T. salignus (Aradottir et al., 2012). ...
... In Europe, the giant willow aphid has established in commercially grown bioenergy willow plantations (Aradottir et al., 2012) and various studies have addressed host susceptibility/resistance, as well as host effects on the reproductive performance of the aphid. In the U.K., T. salignus alates displayed no preference amongst potted SRC willow clones (generally varieties of Salix viminalis) positioned randomly in a glasshouse. ...
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The giant willow aphid Tuberolachnus salignus was discovered in New Zealand in late 2013. Despite being a recent addition to the New Zealand fauna, the aphid is already widespread and abundant throughout the country. The giant willow aphid is expected to have negative impacts on host trees, primarily willows (Salix spp.), as has been observed elsewhere. All willows are exotic to New Zealand and a few have formal weed status, however many species are valued for multiple purposes, including flood protection, land stabilization, shelterbelts, and as early season pollen and nectar resources for honey bees. Tuberolachnus salignus presents a unique problem for New Zealand's thriving honey and honey products industries. Bees readily forage on the vast quantities of honeydew secreted by the aphid, however the honeydew contains melezitose sugar. The low solubility of this sugar results in honey crystallizing in the comb, making it difficult to extract and thereby reducing yield. It is also considered to be poor food for bees, and has been linked to bee dysentery and low overwintering survival. We elaborate on the potential complications for New Zealand as a result of the arrival of this new species and present options for its control and management.
... The combination of sexual and asexual reproduction not only ensures a larger population via short and rapid breeding in stable conditions (Wang, 2011), but also enhances the genetic diversity in harsh environments by genetic recombination via sexual reproduction (Kondrashov, 1988;Hamilton et al., 1990;West et al., 1999). Asexual individuals, in contrast, have a superior colonizing ability (Lynch, 1984), and asexual reproduction in aphids can ensure identity between mother and daughter, generating a high frequency of identical genotypes and keeping levels of genetic diversity low even over large distances (Wilson et al., 1999;Delmotte et al., 2002;Aradottir et al., 2012;Piffaretti et al., 2013;Nibouche et al., 2014). We therefore predict that, due to its parthenogenesis, T. salignus will exhibit lower genetic diversity than C. saliniger. ...
... We further confirmed this pattern by AMOVA, which showed the largest variation component to be among populations (mtDNA, 80.39%; nDNA, 71.55%) and haplogroups (mtDNA, 77.77%; nDNA, 92.59%) for C. saliniger, whereas the largest variation in the nDNA occurred within populations for T. salignus (91.29%), with only 63.77% of variation in the mtDNA among populations (Tables 2 & 3). A similar pattern for T. salignus has been observed in other countries using microsatellite markers, and has been attributed to the species' parthenogenetic reproduction (Aradottir et al., 2012). ...
... Various attempts have been made to link the genetic variation patterns with these biological features of aphids (W€ ohrmann & Hales, 1989;Simon & Hebert, 1995). As we predicted, the low genetic diversity in T. salignus was mainly attributed to its reproduction by parthenogenesis (Blackman & Spence, 1996;Aradottir et al., 2012), whereas the effective recombination that occurs during sexual reproduction increases the genetic diversity in C. saliniger (Kondrashov, 1988;Hamilton et al., 1990;West et al., 1999). The differing patterns of population variation within each species are probably related to their different dispersal abilities and host ranges. ...
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Animals' phylogeographical patterns are frequently explained by Pleistocene glacial fluctuations and topographical environments. However, species-specific biological traits are thought to have profound impacts on distribution patterns, particularly in aphids. We hypothesize that the phylogeographical patterns and/or population dynamics of two sympatric aphids may be different due to their different reproductive modes and feeding sites, even though they share the same hosts and environmental conditions.
... Tuberolachnus salignus (Aradottir et al. 2012). ...
... So these indexes are only conclusive when clonal reproduction is predominant, i.e. for purely clonal lineages or "cryptic sex", but it is difficult to discern sexual lineages from lineages exhibiting intermediate reproductive modes. In aphids, some of these predictions were supported by population genetic studies in several species, for instance: Rhopalosiphum padi (Delmotte et al. 2002), Myzus persicae (Vorburger, Lancaster, et Sunnucks 2003), Sitobion avenae (Papura et al. 2003), Acyrthosiphon pisum (Kanbe et Akimoto 2009), Aphis fabae (Sandrock, Razmjou, et Vorburger 2011), Aphis gossypii (Thomas, Boissot, et Vanlerberghe-Masutti 2012), Tuberolachnus salignus (Aradottir et al. 2012). Aphids reproductive mode can also be studied by experimental induction of sexual phases (Lees 1959;Voegtlin and Halbert 1998). ...
Thesis
Brachycaudus helichrysi est un puceron ravageur des cultures qui inflige de sérieux dégâts à ses hôtes primaires (arbres fruitiers du genre Prunus) ainsi qu'à plusieurs herbacées cultivées correspondant à ses hôtes secondaires (par exemple les tournesols et les chrysanthèmes). L'étude phylogéographique de l'espèce basée sur un échantillonnage mondial, montre que B. helichrysi rassemble deux taxa appelés B. helichrysi H1 et H2. Cette étude, basée sur plusieurs marqueurs génétiques (mitochondriaux, nucléaire et bactériens), révèle une divergence génétique de l'ordre de celle observée entre espèce du genre Brachycaudus. Ceci suggère que B. helichrysi H1 et H2 sont deux espèces sœurs. Comme H1 et H2 sont morphologiquement indistinguables, nous avons mis au point un test de discrimination génétique par PCR-RFLP. L'analyse des génotypes (14 loci microsatellites) combinés aux données écologiques suggère que ces deux espèces sœurs ont des histoires évolutives différentes. Le cycle de vie de B. helichrysi H1 correspondrait à la parthénogenèse cyclique, utilisant les pruniers comme hôte primaire. Nous avons montré qu'il existe chez H1 des clusters génétiques structurés géographiquement. Au contraire, B. helichrysi H2 rassemble principalement des lignées clonales polyphages, persistantes et largement distribuées dans le monde (i.e. superclones), ainsi qu'une lignée sexuée, probablement hétéroécique, qui a été trouvée sur pêchers en Inde. Les individus des deux espèces colonisent fréquemment une même plante herbacée, composant ainsi des colonies « mixtes ». Cette étude apportera un éclairage sur comment l'évolution des cycles de vie, en particulier la perte de la reproduction sexuée, a pu jouer un rôle dans les processus de spéciation au sein du complexe B. helichrysi.
... The same results are also reported for other species of pest aphids (e.g. Sunnucks et al., 1996;Miller et al., 2003;Vorburger et al., 2003;Vorwerk & Forneck, 2006;Aradottir et al., 2012). ...
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The cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae), is a serious pest of citrus in northern Iran, both because of the damaged caused by its feeding and as a vector of several viruses. The genetic structure of populations of A. gossypii on citrus trees at eight localities in Iran was surveyed using seven polymorphic microsatellite loci. Of 240 individuals tested, 142 multilocus genotypes (MLGs) were identified. The presence of multicopy genotypes and negative FIS values revealed that the major mode of reproduction in northern Iran is obligate parthenogenesis. The genotypic diversity of populations ranged between 0.24 and 0.93. Considerable genotypic diversity and a high frequency of unique MLGs, confirmed there is some cyclical parthenogenesis in the region. The analysis of molecular variance revealed high intrapopulation and weak interpopulation genetic differentiation (overall FST = 0.036) among the different populations. The UPGMA dendrogram of eight populations based on Nei's genetic distance indicated two clusters: genotypes from West of Mazandaran and Guilan provinces and those from East of Mazandaran. The same results were also obtained from the STRUCTURE analysis of these populations. This information on the genetic diversity of populations of A. gossypii in northern Iran could be useful for improving the Integrated Pest Management of this aphid. © Institute of Entomology, Biology Centre, Czech Academy of Sciences, České Budějovice.
... However, all these indices are only conclusive when clonal reproduction predominates (Balloux et al. 2003;De Meeûs & Balloux 2004). Some of these predictions have been supported by population genetic studies in several aphid species, including Rhopalosiphum padi (Linnaeus) (Delmotte et al. 2002), Myzus persicae (Vorburger et al. 2003), S. avenae (Papura et al. 2003), A. pisum (Kanbe & Akimoto 2009), Aphis fabae Scopoli (Sandrock et al. 2011), A. gossypii (Thomas et al. 2012 and Tuberolachnus salignus (Gmelin) (Aradottir et al. 2012). The mode of reproduction in aphids can also be studied by the experimental induction of sexual phases (Lees 1959;Voegtlin & Halbert 1998). ...
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DNA degradation, low DNA concentrations and primer-site mutations may result in the incorrect assignment of microsatellite genotypes, potentially biasing population genetic analyses. MICRO-CHECKER is WINDOWS(R)-based software that tests the genotyping of microsatellites from diploid populations. The program aids identification of genotyping errors due to nonamplified alleles (null alleles), short allele dominance (large allele dropout) and the scoring of stutter peaks, and also detects typographic errors. MICRO-CHECKER estimates the frequency of null alleles and, importantly, can adjust the allele and genotype frequencies of the amplified alleles, permitting their use in further population genetic analysis.
Article
We evaluate the cost of sex in cyclical parthenogens coexisting with obligate parthenogens that produce a few sexuals, a situation found in numerous species. In aphids and cladocera, sex is generally the only way to produce a resistant form; this gives a potential ecological advantage to sex. We focus on the selective factor constituted by variations of the environment, that may be alternatively advantageous to cyclical parthenogens (cold winters in aphids, drought in daphnia) or to obligate parthenogens. Our calculations show that the production of a few sexuals by lineages that are essentially obligate parthenogens has a critical effect on the balance between the different life-cycles, especially when this production is limited to males. This male production by intermediates confers additional fitness to obligate parthenogenesis genes and then sharply increases the cost of sex.
Article
Many theories attempt to explain why sexual reproduction has invaded life so thoroughly. Some are plausible, but there remains a need for evolutionary biologists to identify the main factor(s) accounting for the maintenance of sex in diverse, real organisms. An increasing focus of studies on the evolution of sex concerns cyclical parthenogens and aphids in particular, which conveniently show coexistence of sexual and asexual reproductive modes. Recent research has shown a major short-term advantage of sex in aphids to be purely ecological: the production of cold-resistant eggs. However, this is unlikely to be the only force acting to maintain sex in aphids. In the past five years, theoretical developments and the accumulation of ecological and molecular data have greatly advanced understanding of the genetic and evolutionary consequences of reproductive modes in aphids and their distributions in nature, and they have provided tools that promise to make aphids important organisms with which to examine general advantages of sex.
Article
Provides a comprehensive species-by-species account of all the world's tree-dwelling aphids (1758 species). An introductory section gives notes on aphid life cycles, polymorphism and the association between aphids and trees. The second section begins with information on morphology and key characters, a list of the plant families with tree genera from which aphids are recorded is then provided. Host lists and keys for each tree genus make up the bulk of this section. The section concludes with a key to the 23 species of polyphagous aphids which are found on various tree genera. Secion three contains information on the aphids listed and keyed in the previous section, comprising: appearance in life; body length of one or more morphs; host plants; distribution; life cycle, including time of appearance of sexual morphs if known; parasitoids; references to the biology and economic importance; and chromosome number where known. Section four consists of a brief coverage of techniques: collecting; preservation and mounting; and labelling and storage. Thirty-seven pages of references are included in the bibliography. The volume concludes with a collection of photographs of slide-mounted aphids. -S.R.Harris
Article
Darwinian theory has yet to explain adequately the fact of sex. If males provide little or no aid to offspring, a high (up to 2-fold) extra average fitness has to emerge as a property of a sexual parentage if sex is to be stable. The advantage must presumably come from recombination but has been hard to identify. It may well lie in the necessity to recombine defenses to defeat numerous parasites. A model demonstrating this works best for contesting hosts whose defense polymorphisms are constrained to low mutation rates. A review of the literature shows that the predictions of parasite coevolution fit well with the known ecology of sex. Moreover, parasite coevolution is superior to previous models of the evolution of sex by supporting the stability of sex under the following challenging conditions: very low fecundity, realistic patterns of genotype fitness and changing environment, and frequent mutation to parthenogenesis, even while sex pays the full 2-fold cost.
Article
In a previous study, samples of the grain aphid Sitobion avenae (F.) were collected from wheat and adjacent cocksfoot hosts in a population thought to be primarily parthenogenetic, and DNA from individual aphids was analysed with a multilocus technique. Here we have applied single-locus microsatellites and a mitochondrial DNA marker to a subset of the same DNA extracts, and have made several additional inferences about important genetic and population processes in S. avenae. Microsatellite analysis indicated very high levels of genic and genotypic variation. S. avenae fell into three genotypic groups inferred to be almost noninterbreeding, while analysis of linkage and Hardy-Weinberg equilibria suggested high levels of sexual recombination within each genotypic group. Host specialization was evident: one lineage was found only on wheat, and one (bearing many alleles inferred to be introgressed from the blackberry-grass aphid S. fragariae (Walker)) was found only on cocksfoot. The third group of interrelated genotypes was found commonly on both hosts. Although most genotypes were found only once, some were much more numerous in the sample than expected from the frequency of the alleles they contained. This, and rapid temporal changes in genotypic composition of samples, indicates strong selective differences between genotypes and lineages. In the major genotypic group, the commonest genotypes were significantly more homozygous than were rare ones: thus these data may help to explain the frequent observation of homozygous excess in aphid allozymes. The genotype group showing S. avenae-like as well as S. fragariae-like alleles also carried S. fragariae-like mitochondrial DNA in at least 25/31 cases, indicating gender-asymmetrical hybridization.
Article
As French populations of the aphid Sitobion avenae exhibit a range of reproductive modes, this species provides a good opportunity for studying the evolution of breeding system variation. The present analysis combined ecological and genetic investigations into the spatial distribution of variation in reproductive mode. Reproductive mode was characterized in 277 lineages of S. avenae from France, and these aphids were scored for five microsatellite loci. The analyses revealed strong geographical partitioning of breeding systems, with obligate asexuals mostly restricted to the south of France, while lineages producing sexual forms were more common in the north. Contrary to what might be anticipated for organisms with frequent parthenogenesis, there was substantial genic and genotypic diversity, even in the obligately asexual lineages. More than 120 different genotypes were detected among the 277 aphid lineages, with an average of 5.9 alleles per locus (range four to 16) and heterozygosity of 56.7%. As with previous studies of allozyme variation in aphids, most loci showed heterozygote deficits, and disequilibrium was common among allelic variants at different loci, even after removal of replicate copies of genotypes that might have been derived through clonal reproduction. Our results suggest that selection is important in structuring reproductive systems and genetic variation in French S. avenae. Canonical correspondence analysis was employed to examine the associations between genotypic and phenotypic variables, enabling the identification of alleles correlated with life-history traits.
Article
In sharp contrast to their southeast Asian and European counterparts, Sitobion miscanthi and S. near fragariae aphids in Australia exhibit a complete absence of sexual reproduction. This demands an explanation within the context of the evolution and maintenance of sex and parthenogenesis. Accordingly, we executed a genetic analysis of the two species in neighbouring New Zealand. Microsatellites and single-stranded conformation polymorphism/sequence analysis of the nuclear gene elongation factor 1alpha were used to identify aphid clones and confirm species identification, respectively. Karyotypic variation was also investigated. The New Zealand fauna showed few (nonrecombining) genotypes and appears to have received migrants from both Australia and Asia. Other genotypes have apparently arisen in situ in New Zealand, exhibiting stepwise mutation of microsatellite alleles and also karyotypic change. Thus, these data represent rare evidence of evolution within wild-living parthenogenetic lineages. Karyotypic changes appear to occur at a rate even greater than that of microsatellite evolution. Strong geographical partitioning of genotypes/karyotypes was found, with certain ones predominating over large areas. These data suggest that clonal selection could be important in the distribution and patterning of genetic variation. We present a model to explain the genetic patterns, with particular reference to the absence of sexual reproduction in Sitobion aphids in New Zealand and Australia.
Article
Aphis gossypii is an aphid species that is found throughout the world and is extremely polyphagous. It is considered a major pest of cotton and cucurbit species. In Europe, A. gossypii is assumed to reproduce exclusively by apomictic parthenogenesis. The present study investigates the genetic diversity of A. gossypii in a microgeographic, fragmented habitat consisting of eight glasshouses of cucurbit crops. This analysis, which was based on the results from seven microsatellite loci, has confirmed that A. gossypii populations in southern France are primarily asexual, as only 12 nonrecombinant genotypic classes (clones) were identified from 694 aphids. Moreover, a high proportion of the aphids (87%) had one of three common genotypes. No significant correlation was found between genotypic class and host plant species. Within a glasshouse population of A. gossypii, a significant reduction in clonal diversity was observed as the spring/summer season progressed. The final predominance of a clone could result from interclonal competition. At the microgeographic level (i.e. glasshouses within a 500-m radius), significant genetic subdivision was detected and could be attributed to founder effects and the limitation of gene flow imposed by the enclosed nature of the glasshouse structure. Finally, the three common clones of A. gossypii detected in 1996 reappeared in spring 1997 following the winter extinction, together with rare clones that had not previously been seen. The probability that A. gossypii overwinters within refuges at a microgeographic scale from which populations are renewed each spring is discussed.
Article
Aphids are particularly interesting models in the study of genetic and demographic components of plant adaptation because of their breeding system which combines parthenogenesis and sexual reproduction (i.e. cyclical parthenogenesis), and the frequent emergence of host-adapted races reported in this group. In this paper, patterns of host adaptation were assessed on local populations of the aphid Sitobion avenae by following their demographic and genetic structure in a maize field for two consecutive years. The existence of putative generalist (polyphagous) or specialized (host-adapted) genotypes was also investigated by comparing the genotypic distribution of this aphid on maize and other cultivated host plants, using five microsatellite loci. Although population dynamics revealed strong variation in aphid abundance during the colonization period on maize, two genotypes identified at seven additional microsatellite loci were predominant and exhibited stable frequencies over cropping season and between years. Based on present and earlier studies, these two prevalent genotypes were shown to survive on different host plants other than maize, to colonize large geographical zones and to persist parthenogenetically for several years. All these data strongly suggest that these two genotypes are asexual generalist clones that could have been favoured by agricultural practices encountered in western Europe. Besides these two clones, a continual replacement of rare genotypes was observed on maize in both years. Hypotheses involving selection via aphid-plant interactions and natural enemies were proposed for explaining the disappearance of these genotypes on maize.
Article
Cyclical parthenogens, including aphids, are attractive models for comparing the genetic outcomes of sexual and asexual reproduction, which determine their respective evolutionary advantages. In this study, we examined how reproductive mode shapes genetic structure of sexual (cyclically parthenogenetic) and asexual (obligately parthenogenetic) populations of the aphid Rhopalosiphum padi by comparing microsatellite and allozyme data sets. Allozymes showed little polymorphism, confirming earlier studies with these markers. In contrast, microsatellite loci were highly polymorphic and showed patterns very discordant from allozyme loci. In particular, microsatellites revealed strong heterozygote excess in asexual populations, whereas allozymes showed heterozygote deficits. Various hypotheses are explored that could account for the conflicting results of these two types of genetic markers. A strong differentiation between reproductive modes was found with both types of markers. Microsatellites indicated that sexual populations have high allelic polymorphism and heterozygote deficits (possibly because of population subdivision, inbreeding or selection). Little geographical differentiation was found among sexual populations confirming the large dispersal ability of this aphid. In contrast, asexual populations showed less allelic polymorphism but high heterozygosity at most loci. Two alternative hypotheses are proposed to explain this heterozygosity excess: allele sequence divergence during long-term asexuality or hybrid origin of asexual lineages. Clonal diversity of asexual lineages of R. padi was substantial suggesting that they could have frozen genetic diversity from the pool of sexual lineages. Several widespread asexual genotypes were found to persist through time, as already seen in other aphid species, a feature seemingly consistent with the general-purpose genotype hypothesis.
Article
Cyclically parthenogenetic organisms may have facultative asexual counterparts. Such organisms, including aphids, are therefore interesting models for the study of ecological and genetic interactions between lineages differing in reproductive mode. Earlier studies on aphids have revealed major differences in the genetic outcomes of populations that are possibly resulting mostly either from sexual or from asexual reproduction. Besides, notable gene flow between sexual and asexual derivatives has been suspected, which could lead to the emergence of new asexual lineages. The present study examines the interplay between these lineages and is based on analyses of population structure of individuals that may contribute to the pool of sexual reproductive forms in the host alternating aphid Rhopalosiphum padi. Using a Bayesian assignment method, we first show that the sexual forms of R. padi on mating sites encompass two genetically distinct clusters of individuals in the western part of France. The first cluster included unique genotypes of sexual lineages, while the second cluster included facultatively asexual lineages in numerous copies, the reproductive mode of the two clusters being confirmed by reference clones. Sexual reproductive forms produced by sexual and facultatively asexual lineages are thus admixed at mating sites which gives a large opportunity for the two clusters to mate with each other. Nevertheless, this study also highlights, as previously demonstrated, that the two clusters retained high genetic differentiation. Possible explanations for the inferred limited genetic exchanges are advanced in the discussion, but further dedicated investigations are required to solve this paradox.
Article
The peach-potato aphid Myzus persicae (Sulzer) is an important vector of plant viruses. A network of suction traps collects aerial samples of this aphid in order to monitor and help predict its spatial distribution and likely impact on virus transmission in crops. A suction trap catch is thought to be a good representation of the total aphid pool. Sensitive molecular markers have been developed that determine the genetic composition of the M. persicae population. In Scotland, UK, these were applied to field collections revealing a limited number of clones. Molecular markers are less successful when applied to specimens that have been preserved in an ethanol-based trap fluid designed to preserve morphology. An assessment of different DNA extraction and PCR techniques is presented and the most efficient are used to analyse M. persicae specimens caught in the Dundee suction trap in 2001, a year when exceptionally high numbers were caught. The results reveal that the majority of the M. persicae caught belonged to two highly insecticide resistant clones. In addition, it was possible to compare the relative frequencies of genotypes caught in the trap with those collected at insecticide treated and untreated field sites in the vicinity. These results indicate that, in addition to suction trap data, the ability to sample field sites provides valuable early warning data which have implications for pest control and virus management strategies.
Article
Bioenergy from plants, particularly from perennial grasses and trees, could make a substantial contribution to alleviation of global problems in climate change and energy security if high yields can be sustained. Here, yield traits in a range of key bioenergy crops are reviewed, from which several targets for future improvement can be identified. Some are already the focus of genetically modified (GM) and non-GM approaches. However, the efficient growth strategies of perennial bioenergy crops rely on newly assimilated and recycled carbon and remobilized nitrogen in a continually shifting balance between sources and sinks. This balance is affected by biotic (e.g. pest, disease) and abiotic (e.g. drought) stresses. Future research should focus on three main challenges: changing (photo)thermal time sensitivity to lengthen the growing season without risking frost damage or limiting remobilization of nutritional elements following senescence; increasing aboveground biomass without depleting belowground reserves required for next year's growth and thus without increasing the requirement for nutrient applications; and increasing aboveground biomass without increasing water use.
Population biology and host selection of the giant willow aphid
  • G I Aradottir
Aradottir, G.I. (2010) Population biology and host selection of the giant willow aphid ( Tuberolachnus salignus Gmelin). PhD Thesis, University of London.
Microsatellite markers for the giant willow aphid (Tuberolachnus salignus Gmelin).
  • Aradottir
Aradottir, G.I. & Hanley, S.J. (2010) Microsatellite markers for the giant willow aphid (Tuberolachnus salignus Gmelin). Molecular Ecology Resources, 10, 1106-1108.
Aphids on the World's Trees, An Identification and Information Guide. CAB International in Association with The Natural History Museum
  • R L Blackman
  • V F Eastop
Blackman, R.L. & Eastop, V.F. (1994) Aphids on the World's Trees, An Identification and Information Guide. CAB International in Association with The Natural History Museum, U.K.
R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Austria
  • R Development
  • Core Team
R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Austria. http://www.r-project.org/ [accessed on 22 November 2011].
Sexual reproduction as an adaptation to resist parasites (a review)
  • W D Hamilton
  • R Axelrod
  • R Tanese
Hamilton, W.D., Axelrod, R. & Tanese, R. (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences of the United States of America, 87, 3566-3573.
Sexual reproduction as an adaptation to resist parasites (a review).
  • Hamilton