Browsing by Author "Loxdale, Hugh D."

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    The 'Cake on the plate' syndrome ... and how specialist tansy aphids avoid extinction by hungry predators and parasitoids: insights from the use of polymorphic microsatellite markers
    (2016-07) Nyabuga, Franklin N.; Loxdale, Hugh D.; Weisser, Wolfgang W.
    It was initially shown from 12.2 m high suction trap aerial density data and later confirmed using polymorphic molecular markers (initially allozymes, later high resolution DNA markers, especially microsatellites), that different species of aphids (Hemiptera: Aphididae) have different migratory urges and abilities. Such population genetic differences are manifested in the different patterns obtained for different species: thus highly migratory species (e.g. the grain aphid, Sitobion avenae F.) display similar allele frequencies patterns over large geographical distances, apparently intermediate migrants (e.g. blackberry-grain aphid, S. fragariae (Walker) and damson-hop aphid, Phorodon humuli (Schrank)) show much more local heterogeneity, whilst relatively very ‘immobile’ species like specialist tansy aphids (i.e. Macrosiphoniella tanacetaria (Kaltenbach) and Metopeurum fuscoviride Stroyan), which have a metapopulation structure, show highly heterogeneous patterns, even at small spatial scales (see Loxdale & Lushai, 2007 for a review and Massonnet, 2002). If it is indeed true that different aphid species do have different levels of ‘migratoriness’ manifested as migratory range or ambit, then this may well impact on the ecology and population genetics of the predators, wasp parasitoids and pathogens that attack them. That different aphids migrate differentially is also no doubt related to the abundance and distribution of their host plant/s (e.g. Cammel et al., 1989) and hence the ease with which the insects not only reproduce but also find new plants when undergoing inter-host migrations during the spring, summer and autumn. The latter often involves in holocyclic species (i.e. with annual sexual phase in which a cold hardy overwintering egg is produced), winged pre-sexual or sexual forms and sometimes, host alternation between a herbaceous spring-summer host and a primary woody host (Dixon, 1998). It is calculated that in the case of the bird cherry-oat aphid, Rhopalosiphum padi (L.), only about 0.6% of returning autumn winged migrants find the primary overwintering host bird cherry, Prunus padus, and hence can mate and thereby successfully overwinter to produce the next generations (Ward et al., 1998). Below the boundary level of still air, aphids home in on their hosts using visual and olfactory cues (Dixon, 1998; Irwin et al., 2007). Sexual females have been reported to use pheromones to attract the migrating autumn males (e.g. Pope et al., 2007). The wasp parasitoids (Hymenoptera: Braconidae: Aphidiidae) also use both host plant and aphid cues to find their hosts (Godfray, 1994), and presumably must therefore, where host alternating aphids are concerned, change their behaviour from actively searching on a secondary host/s
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    The 'Cake on the plate' syndrome ... and how specialist tansy aphids avoid extinction by hungry predators and parasitoids: insights from the use of polymorphic microsatellite markers
    (2008) Nyabuga, Franklin N.; Loxdale, Hugh D.; Weisser, Wolfgang W.
    It was initially shown from 12.2 m high suction trap aerial density data and later confirmed using polymorphic molecular markers (initially allozymes, later high resolution DNA markers, especially microsatellites), that different species of aphids (Hemiptera: Aphididae) have different migratory urges and abilities. Such population genetic differences are manifested in the different patterns obtained for different species: thus highly migratory species (e.g. the grain aphid, Sitobion avenae F.) display similar allele frequencies patterns over large geographical distances, apparently intermediate migrants (e.g. blackberry-grain aphid, S. fragariae (Walker) and damson-hop aphid, Phorodon humuli (Schrank)) show much more local heterogeneity, whilst relatively very ‘immobile’ species like specialist tansy aphids (i.e. Macrosiphoniella tanacetaria (Kaltenbach) and Metopeurum fuscoviride Stroyan), which have a metapopulation structure, show highly heterogeneous patterns, even at small spatial scales (see Loxdale & Lushai, 2007 for a review and Massonnet, 2002). If it is indeed true that different aphid species do have different levels of ‘migratoriness’ manifested as migratory range or ambit, then this may well impact on the ecology and population genetics of the predators, wasp parasitoids and pathogens that attack them. That different aphids migrate differentially is also no doubt related to the abundance and distribution of their host plant/s (e.g. Cammel et al., 1989) and hence the ease with which the insects not only reproduce but also find new plants when undergoing inter-host migrations during the spring, summer and autumn. The latter often involves in holocyclic species (i.e. with annual sexual phase in which a cold hardy overwintering egg is produced), winged pre-sexual or sexual forms and sometimes, host alternation between a herbaceous spring-summer host and a primary woody host (Dixon, 1998). It is calculated that in the case of the bird cherry-oat aphid, Rhopalosiphum padi (L.), only about 0.6% of returning autumn winged migrants find the primary overwintering host bird cherry, Prunus padus, and hence can mate and thereby successfully overwinter to produce the next generations (Ward et al., 1998). Below the boundary level of still air, aphids home in on their hosts using visual and olfactory cues (Dixon, 1998; Irwin et al., 2007). Sexual females have been reported to use pheromones to attract the migrating autumn males (e.g. Pope et al., 2007). The wasp parasitoids (Hymenoptera: Braconidae: Aphidiidae) also use both host plant and aphid cues to find their hosts (Godfray, 1994), and presumably must therefore, where host alternating aphids are concerned, change their behaviour from actively searching on a secondary host/s
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    Coevolutionary fine-tuning: evidence for genetic tracking between a specialist wasp parasitoid and its aphid host in a dual metapopulation interaction
    (Cambridge University Press, 2012-04) Nyabuga, Franklin N.; Loxdale, Hugh D.; Heckel, David G.; Weisser, Wolfgang W.
    In the interaction between two ecologically-associated species, the population structure of one species may affect the population structure of the other. Here, we examine the population structures of the aphid Metopeurum fuscoviride, a specialist on tansy Tanacetum vulgare, and its specialist primary hymenopterous parasitoid Lysiphlebus hirticornis, both of which are characterized by multivoltine life histories and a classic metapopulation structure. Samples of the aphid host and the parasitoid were collected from eight sites in and around Jena, Germany, where both insect species co-occur, and then were genotyped using suites of polymorphic microsatellite markers. The host aphid was greatly differentiated in terms of its spatial population genetic patterning, while the parasitoid was, in comparison, only moderately differentiated. There was a positive Mantel test correlation between pairwise shared allele distance (DAS) of the host and parasitoid, i.e. if host subpopulation samples were more similar between two particular sites, so were the parasitoid subpopulation samples. We argue that while the differences in the levels of genetic differentiation are due to the differences in the biology of the species, the correlations between host and parasitoid are indicative of dependence of the parasitoid population structure on that of its aphid host. The parasitoid is genetically tracking behind the aphid host, as can be expected in a classic metapopulation structure where host persistence depends on a delay between host and parasitoid colonization of the patch. The results may also have relevance to the Red Queen hypothesis, whereupon in the ‘arms race’ between parasitoid and its host, the latter ‘attempts’ to evolve away from the former.
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    Microsatellites from Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae), a specialist primary parasitoid attacking the specialist tansy aphid, Metopeurum fuscoviride Stroyan (Hemiptera: Aphididae)
    (Blackwell Publishing Ltd, 2009-04) Loxdale, Hugh D.; Sharbel, Tomothy F.; Todd, Mark; Weisser, Wolfgang W.
    Nine polymorphic microsatellite loci were isolated from the specialist aphid parasitoid, Lysiphlebus hirticornis. In addition, two published loci from closely related Lysiphlebus species were also used. Allelic diversity and heterozygosity were quantified in samples collected from eight tansy plants growing in an area of approximately 150m2 in Jena, Germany.
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    Spatial population dynamics of a specialist aphid parasitoid, Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae: Aphidiinae): evidence for philopatry and restricted dispersal
    (Macmillan Publishers Limited, 2010-01) Nyabuga, Franklin N.; Loxdale, Hugh D.; Heckel, David G.; Weisser, Wolfgang W.
    Within insect communities, the population ecology of organisms representing higher trophic levels, for example, hymenopterous parasitoids, may be influenced by the structure of their insect hosts. Using microsatellite markers and ecological data, we investigated the population structure of the specialist braconid wasp parasitoid, Lysiphlebus hirticornis Mackauer attacking Metopeurum fuscoviride, a specialist aphid feeding on tansy, Tanacetum vulgare. Previous studies revealed that M. fuscoviride has a classic metapopulation structure with high subpopulation turnover. In this study, up to 100% of ramets within a host plant genet colonized by aphids were colonized by the parasitoid, yet plants with aphids but no parasitoids were also observed. Genetic differentiation measured by FST, actual differentiation (D) and relative differentiation (GST) indicated highly structured parasitoid population demes, with restricted gene flow among and between parasitoid subpopulations at the various sites. Interestingly, both field data and population assignment analysis showed that the parasitoid is highly philopatric. Thus, despite the frequent local extinctions of the aphid host, the parasitoid continuously exploits its aphid host and contributes to the demise of local aphid subpopulations, rather than spreading its genes over many aphid populations. FST values for the haplodiploid parasitoid were similar to those found in an independent study of the diploid aphid host, M. fuscoviride, hence supporting the view that an insect herbivore’s population structure directly influences the ecology and genetics of the higher trophic level, in this case the wasp parasitoid. Heredity (2010) 105, 433–442; doi:10.1038/hdy.2009.190; published online 27 January 2010
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    Stay at home aphids: comparative spatial and seasonal metapopulation structure and dynamics of two specialist tansy aphid species studied using microsatellite markers
    (The Linnean Society of London, 2011-06) Nyabuga, Franklin N.; Loxdale, Hugh D.; Schöfl, Gerhard; Wiesner, Kerstin R.; Heckel, David G.; Weisser, Wolfgang W.
    Two tansy-feeding aphids, Macrosiphoniella tanacetaria (MA) and Metopeurum fuscoviride (ME), were studied at a small spatial scale in and around Jena (< 80 km2) using polymorphic microsatellite markers. Both species were found in approximately 60% of sites formerly known to harbour the aphids, although, generally when they did occur, they occurred singly (MA ~50%; ME ~60%) and rarely together on the same plant at the same time (approximately 10%) and then usually only in the early part of the growing season. This difference may be a result of quasi-apparent competition effects elicited by ants farming ME aphids, and preferentially actively eliminating or disturbing MA aphids. In terms of population genetics, both aphids showed extreme genetic heterogeneity within a metapopulation structure, with ME more than MA (i.e. higher FST values, approximately 0.4 versus 0.15, respectively), and limited levels of interpopulation gene flow. Subpopulations often deviated from Hardy–Weinberg equilibrium and showed linkage disequilibria, as expected in animals with extended parthenogenetic reproduction, and had positive FIS values for most large samples, suggesting inbreeding, and possibly philopatry, certainly in ME. Hierarchical analysis (allele range and number per locus, analysis of molecular variance and FST) strongly suggested that the plant rather than site governs the level of genetic variation. Bayesian clustering analysis revealed that both species had heterogeneous historical genetic patterning, with K (number of subgroups) in the range 3–7. Evidence is also provided from isolation-by-distance and private allele analyses indicating that, in MA, the presence of winged autumnmales, absent in ME where males are wingless, influences comparative population genetic structuring, such that ME subpopulations are comparatively more inbred and genetically differentiated than MA subpopulations. Lastly, additional spatial arrangement (ALLELES-IN-SPACE) analysis showed that, in both species, certain subpopulations were genetically isolated from the remainder, probably as a result of geographical barriers, including intervening buildings and woods. As such, the biology of these tansy aphids living in semi-natural habitats is very different from many pest aphid species examined within agro-ecosystems and infesting ephemeral crops. This is because the former appear to be much more reluctant to fly and hence show contrastingly much higher levels of interpopulation divergence, even at small spatial scales as investigated in the present study. Indeed, the number of genotypic clusters found for tansy aphids using Bayesian approaches is similar to that globally for the major pest, the peach-potato aphid, Myzus persicae. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 838–865.
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    Temporal genetic structuring of a specialist parasitoid, Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae) attacking a specialist aphid on tansy
    (The Linnean Society of London, 2011) Nyabuga, Franklin N.; Loxdale, Hugh D.; Heckel, David G.; Weisser, Wolfgang W.
    In insect species characterized by inbreeding, limited dispersal, and a metapopulation structure, high genetic differentiation and reduced genetic diversity within local populations are expected. Using the model system Lysiphlebus hirticornis Mackauer, a specialist parasitoid of the tansy aphid, Metopeurum fuscoviride Stroyan (Hemiptera: Aphididae), we examined within-site temporal population dynamics and genetics, including molecular variation at the tansy plant level. Aphid-parasitoid dynamics were surveyed and parasitoids sampled from 72 tansy plants at 11 sites in and around Jena, Germany, over one growing season. Thereafter, parasitoid samples were genotyped at 11 polymorphic microsatellite loci. Colonization, extinction, and recolonization events occurred during the season. Allele numbers and identities were highly variable over time. When samples from all sites were pooled, allele number over all loci showed a decreasing trend with time. At the level of sites, temporal changes in genetic diversity were more variable. Analysis of molecular variance revealed that samples at the plant level explained the highest variance compared to at site level. We conclude that the genetic structuring of this insect is very fine grained (i.e. at the tansy plant level) and the temporal genetic diversity is explained by a combination of extinction and recolonization events, as well as inbreeding.