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  1. Home
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Browsing by Author "Nyabuga, Franklin N."

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    Annotations of novel antennae-expressed genes in male Glossina morsitans morsitans tsetse flies
    (Plos 1, 2022-08) Bwana, Billiah K.; Mireji, Paul O.; Obiero, George F.; Gakii, Consolata; Akoth, Modesta O.; Mugweru, Julius N.; Nyabuga, Franklin N.; Wachira, Benson M.; Bateta, Rosemary; Ng’ang’a, Margaret M.; Hassanali, Ahmed
    Tsetse flies use antennal expressed genes to navigate their environment. While most canonical genes associated with chemoreception are annotated, potential gaps with important antennal genes are uncharacterized in Glossina morsitans morsitans. We generated antennae-specific transcriptomes from adult male G. m. morsitans flies fed/unfed on bloodmeal and/or exposed to an attractant (ε-nonalactone), a repellant (δ-nonalactone) or paraffin diluent. Using bioinformatics approach, we mapped raw reads onto G. m. morsitans geneset from VectorBase and collected un-mapped reads (constituting the gaps in annotation). We de novo assembled these reads (un-mapped) into transcript and identified corresponding genes of the transcripts in G. m. morsitans gene-set and protein homologs in UniProt protein database to further annotate the gaps. We predicted potential protein-coding gene regions associated with these transcripts in G. m. morsitans genome, annotated/curated these genes and identified their putative annotated orthologs/homologs in Drosophila melanogaster, Musca domestica or Anopheles gambiae genomes. We finally evaluated differential expression of the novel genes in relation to odor exposures relative to no-odor control (unfed flies). About 45.21% of the sequenced reads had no corresponding transcripts within G. m. morsitans gene-set, corresponding to the gap in existing annotation of the tsetse fly genome. The total reads assembled into 72,428 unique transcripts, most (74.43%) of which had no corresponding genes in the UniProt database. We annotated/curated 592 genes from these transcripts, among which 202 were novel while 390 were improvements of existing genes in the G. m. morsitans genome. Among the novel genes, 94 had orthologs in D. melanogaster, M. domestica or An. gambiae while 88 had homologs in UniProt. These orthologs were putatively associated with oxidative regulation, protein synthesis, transcriptional and/or translational regulation, detoxification and metal ion binding, thus providing insight into their specific roles in antennal physiological processes in male G. m. morsitans. A novel gene (GMOY014237.R1396) was differentially expressed in response to the attractant. We thus established significant gaps in G. m. morsitans genome annotation and identified novel male antennae-expressed genes in the genome, among which > 53% (108) are potentially G. m. morsitans specific.
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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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    Coevolutionary fine-tuning: evidence for genetic tracking between a specialist wasp parasitoid and its aphid host in a dual metapopulation interaction
    (2012-09) Nyabuga, Franklin N.; Loxdale, H. D.; Heckel, D.; Weisser, 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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    Common Cerambycid Pheromone Components as Attractants for Longhorn Beetles (Cerambycidae) Breeding in Ephemeral Oak Substrates in Northern Europe
    (Springer, 2019-06) Molander, Mikael A.; Winde, Inis B.; Burman, Joseph; Nyabuga, Franklin N.; Lindblom, Tobias U. T.; Hanks, Lawrence M.; Millar, Jocelyn G.; Larsson, Mattias C.
    Longhorn beetles are ecologically important insects in forest ecosystems as decomposers of woody substrates, microhabitat engineers, and as components of forest food webs. These species can be greatly affected both positively and negatively by modern forestry management practices, and should be monitored accordingly. Through headspace sampling, coupled gas chromatographyelectroantennography, gas chromatography-mass spectrometry, and field bioassays, we identified two compounds, 2-methyl-1- butanol and 3-hydroxy-2-hexanone, that constitute aggregation-sex pheromone attractants of three cerambycid species which breed primarily in different types of fresh, recently dead oakwood in Northern Europe: Pyrrhidium sanguineum (L.), Phymatodes alni ssp. alni (L.), and Phymatodes testaceus (L.) (Cerambycinae: Callidiini). Analyses of headspace volatiles collected from live insects indicated that the male-produced aggregation-sex pheromone of P. sanguineum is a 1–15:100 blend of (R)-2-methyl-1-butanol and (R)-3-hydroxy-2- hexanone, whereas the corresponding ratios for P. alni were 70–110:100. In field bioassays, adult P. sanguineum and P. alni were significantly attracted to multiple blends with varying ratios of the two compounds. When tested individually, the compounds were minimally attractive. In contrast, adult P. testaceus exhibited nonspecific attraction to both of the individual compounds and to different blends, despite the hydroxyketone not being part of its pheromone, which consists of (R)-2-methyl-1-butanol alone. Overall, our results suggest that a blend of 50:100 of racemic 2-methyl-1-butanol and 3-hydroxy-2-hexanone is appropriate for parallel, cost-efficient pheromone-based monitoring of all three species. In particular, these species could serve as useful indicators of how modern forestry practices affect a whole guild of saproxylic insects that require ephemeral deadwood substrates for successful breeding.
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    Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study
    (2010-05) Nyabuga, Franklin N.; Outreman, Yannick; Simon, Jean-Christophe; Heckel, David G.; Weisser, Wolfgang W.
    In order to reduce parasite-induced mortality, hosts may be involved in mutualistic interactions in which the partner contributes to resistance against the parasite. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), harbours secondary bacterial endosymbionts, some of which have been reported to confer resistance against aphid parasitoids. Although this resistance often results in death of the developing parasitoid larvae, some parasitoid individuals succeed in developing into adults. Whether these individuals suffer from fitness reduction compared to parasitoids developing in pea aphid clones without symbionts has not been tested so far. Using 30 pea aphid clones that differed in their endosymbiont complement, we studied the effects of these endosymbionts on aphid resistance against the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), host–parasitoid physiological interactions, and fitness of emerging adult parasitoids. The number of symbiont species in an aphid clone was positively correlated with a number of resistance measurements but there were also clear symbiont-specific effects on the host–parasitoid interaction. As in previous studies, pea aphid clones infected with Hamiltonella defensa Moran et al. showed resistance against the parasitoid. In addition, pea aphid clones infected with Regiella insecticolaMoran et al. and co-infections of H. defensa–Spiroplasma, R. insecticola–Spiroplasma, and R. insecticola–H. defensa showed reduced levels of parasitism and mummification. Parasitoids emerging from symbiontinfected aphid clones often had a longer developmental time and reduced mass. The number of teratocytes was generally lower when parasitoids oviposited in aphid clones with a symbiont complement. Interestingly, unparasitized aphids infected with Serratia symbiotica Moran et al. and R. insecticola had a higher fecundity than unparasitized aphids of uninfected pea aphid clones. We conclude that in addition to conferring resistance, pea aphid symbionts also negatively affect parasitoids that successfully hatch from aphid mummies. Because of the link between aphid resistance and the number of teratocytes, the mechanism underlying resistance by symbiont infection may involve interference with teratocyte development.
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    Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study
    (2010-05) Nyabuga, Franklin N.; Outreman, Yannick; Jean-Christophe, Simon; Heckel, David G.; Weisser, Wolfgang W.
    In order to reduce parasite-induced mortality, hosts may be involved in mutualistic interactions in which the partner contributes to resistance against the parasite. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), harbours secondary bacterial endosymbionts, some of which have been reported to confer resistance against aphid parasitoids. Although this resistance often results in death of the developing parasitoid larvae, some parasitoid individuals succeed in developing into adults. Whether these individuals suffer from fitness reduction compared to parasitoids developing in pea aphid clones without symbionts has not been tested so far. Using 30 pea aphid clones that differed in their endosymbiont complement, we studied the effects of these endosymbionts on aphid resistance against the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), host–parasitoid physiological interactions, and fitness of emerging adult parasitoids. The number of symbiont species in an aphid clone was positively correlated with a number of resistance measurements but there were also clear symbiont-specific effects on the host–parasitoid interaction. As in previous studies, pea aphid clones infected with Hamiltonella defensa Moran et al. showed resistance against the parasitoid. In addition, pea aphid clones infected with Regiella insecticolaMoran et al. and co-infections of H. defensa–Spiroplasma, R. insecticola–Spiroplasma, and R. insecticola–H. defensa showed reduced levels of parasitism and mummification. Parasitoids emerging from symbiontinfected aphid clones often had a longer developmental time and reduced mass. The number of teratocytes was generally lower when parasitoids oviposited in aphid clones with a symbiont complement. Interestingly, unparasitized aphids infected with Serratia symbiotica Moran et al. and R. insecticola had a higher fecundity than unparasitized aphids of uninfected pea aphid clones. We conclude that in addition to conferring resistance, pea aphid symbionts also negatively affect parasitoids that successfully hatch from aphid mummies. Because of the link between aphid resistance and the number of teratocytes, the mechanism underlying resistance by symbiont infection may involve interference with teratocyte development.
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    Field Abundance Patterns and Odor-Mediated Host Choice by Clover Seed Weevils, Apion fulvipes and Apion trifolii (Coleoptera: Apionidae)
    (2015-02-05) Nyabuga, Franklin N.; Carrasco, David; Ranaker, Lynn; Andersson, Martin N.; Birgersson, Ran; Larsson, Mattias C.; Lundin, Ola; Rundlo, Maj; Svensson, Glenn P.; Anderbrant, Olle; Lankinen, Anda Sa
    The clover seed weevils Apion fulvipes Geoffroy, 1785 and Apion trifolii L., 1768 (Coleoptera: Apionidae) cause major losses to seed production of white clover (Trifolium repens L.) and red clover (Trifolium pratense L.), respectively. Clover is important as animal forage and an alternative to inorganic fertilizers. Because clover is mainly pollinated by bees, the use of insecticides in management of these weevils is discouraged. To gain basic knowledge for development of alternative management strategies, we investigated weevil field abundance over two growing seasons, as well as feeding and olfactory host preferences by A. fulvipes and A. trifolii. Field trap catches in southern Sweden revealed that white clover was dominated by A. fulvipes and red clover by A. trifolii. For both weevil species, female catches were positively correlated to the number of clover buds and flowers in the field. In feeding and olfactory bioassays, females of A. fulvipes and A. trifolii showed a preference for T. repens and T. pratense, respectively. However, the feeding preference was lost when the antennae were removed, indicating a significant role of olfaction in host choice. Male weevils of both species did not show clear olfactory or feeding preferences for host plant species. The field study and laboratory bioassays demonstrate that, at least for female weevils, olfaction is important for selection of host plants.We discuss these novel results in the context of managing these important pests of clover by exploiting olfaction and behavioral attraction to host plant volatiles.
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    Field Abundance Patterns and Odor-Mediated Host Choice by Clover Seed Weevils, Apion fulvipes and Apion trifolii (Coleoptera: Apionidae)
    (2015-02) Nyabuga, Franklin N.
    The clover seed weevils Apion fulvipes Geoffroy, 1785 and Apion trifolii L., 1768 (Coleoptera: Apionidae) cause major losses to seed production of white clover (Trifolium repens L.) and red clover (Trifolium pratense L.), respectively. Clover is important as animal forage and an alternative to inorganic fertilizers. Because clover is mainly pollinated by bees, the use of insecticides in management of these weevils is discouraged. To gain basic knowledge for development of alternative management strategies, we investigated weevil field abundance over two growing seasons, as well as feeding and olfactory host preferences by A. fulvipes and A. trifolii. Field trap catches in southern Sweden revealed that white clover was dominated by A. fulvipes and red clover by A. trifolii. For both weevil species, female catches were positively correlated to the number of clover buds and flowers in the field. In feeding and olfactory bioassays, females of A. fulvipes and A. trifolii showed a preference for T. repens and T. pratense, respectively. However, the feeding preference was lost when the antennae were removed, indicating a significant role of olfaction in host choice. Male weevils of both species did not show clear olfactory or feeding preferences for host plant species. The field study and laboratory bioassays demonstrate that, at least for female weevils, olfaction is important for selection of host plants.We discuss these novel results in the context of managing these important pests of clover by exploiting olfaction and behavioral attraction to host plant volatiles.
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    Impact of low-cost management techniques on population dynamics of plant-parasitic nematodes in sweet potato
    (Elsevier, 2020-07) Maina, Hellen; Karuri, Hannah W.; Rotich, Felix; Nyabuga, Franklin N.
    Sweet potato is an important food security crop but its production is limited by various biotic constraints including plant-parasitic nematodes (PPN). In Kenya, current PPN management practices in sweet potato have several limitations hence the need for alternative low-cost management strategies. This study evaluated the impact of intercropping maize and sweet potato (MS) and application of Tithonia diversifolia (MG), cow (CM) and goat manure (GM) on population dynamics of PPN and the effect on metabolic footprints, ecological and functional indices. Field experiments were established in a randomized complete block design involving the four treatments and unamended controls. Soil samples were collected during long (LR) and short (SR) rains seasons. Forty-seven nematode genera were identified in both seasons. Principle response curves analysis revealed that goat manure had the most pronounced effect on PPN. There were differences in metabolic footprints, ecological and functional indices during LR and SR. In CM plots, predator footprint was high during the long rains season. Functional metabolic footprints categorized all plots as degraded in both seasons except MS which was structured in SR. However, CM bordered a structured ecosystem in both seasons while GM bordered a structured ecosystem in LR. Goat manure may have enhanced the natural ability of soil to regulate PPN affecting sweet potato and it may provide an alternative sustainable method of PPN control for smallholders.
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    Mating Strategies in Solitary Aphid Parasitoids: Effect of Patch Residence Time and Ant Attendance
    (Springer, 2012-01) Nyabuga, Franklin N.; Völkl, Wolfgang; Schwörer, Ulrich; Weisser, Wolfgang W.; Mackauer, Manfred
    Mate finding and dispersal from the natal patch in parasitoid Hymenoptera are influenced by the availability of host resources and interactions with other organisms. We compared the mating behavior of three solitary aphid parasitoids, Aphidius ervi Haliday, Lysiphlebus hirticornis Mackauer and Pauesia pini (Haliday) (Hymenoptera: Braconidae: Aphidiinae) that differ in host resource exploitation and ant mutualism. In L. hirticornis, which is obligately ant-attended, the residence time on the natal patch was approximately 4 h compared with less than 2 h in the facultatively ant-attended P. pini; the sexes did not differ in residence time. Females of A. ervi, which is not attended by ants, stayed for slightly more than 2 h on the natal patch while their male siblings remained for only 1 h. In L. hirticornis, 90% of all siblings in a clutch mated on the natal patch but only 13% in A. ervi and 42% in P. pini did so. Off-patch matings (23%) were observed only in A. ervi. Males and females of L. hirticornis were 12-times more likely to mate on the natal patch when aphids and ants were present than when either of the latter species was removed; and patch residence time declined from approximately 4 h to approximately 2.5 h in the absence of either aphids or ants. We propose that, in aphidiine wasps and perhaps other quasigregarious parasitoids, mating behavior is influenced by the availability of resources on the natal patch and the presence or absence of trophobiotic ants. Partial sib mating is expected in species producing large clutches and having a long patch residence time.
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    Mating Strategies in Solitary Aphid Parasitoids: Effect of Patch Residence Time and Ant Attendance
    (2011-06) Nyabuga, Franklin N.; Völkl, Wolfgang; Schwörer, Ulrich; Wolfgang, W. Weisser; Mackauer, Manfred
    Mate finding and dispersal from the natal patch in parasitoid Hymenoptera are influenced by the availability of host resources and interactions with other organisms. We compared the mating behavior of three solitary aphid parasitoids, Aphidius ervi Haliday, Lysiphlebus hirticornis Mackauer and Pauesia pini (Haliday) (Hymenoptera: Braconidae: Aphidiinae) that differ in host resource exploitation and ant mutualism. In L. hirticornis, which is obligately ant-attended, the residence time on the natal patch was approximately 4 h compared with less than 2 h in the facultatively ant-attended P. pini; the sexes did not differ in residence time. Females of A. ervi, which is not attended by ants, stayed for slightly more than 2 h on the natal patch while their male siblings remained for only 1 h. In L. hirticornis, 90% of all siblings in a clutch mated on the natal patch but only 13% in A. ervi and 42% in P. pini did so. Off-patch matings (23%) were observed only in A. ervi. Males and females of L. hirticornis were 12-times more likely to mate on the natal patch when aphids and ants were present than when either of the latter species was removed; and patch residence time declined from approximately 4 h to approximately 2.5 h in the absence of either aphids or ants. We propose that, in aphidiine wasps and perhaps other quasigregarious parasitoids, mating behavior is influenced by the availability of resources on the natal patch and the presence or absence of trophobiotic ants.
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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)
    (2008-10) Nyabuga, Franklin N.; Wolfgang, W. Weisser; Loxdale, H. D.
    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
    (2010-01) Nyabuga, Franklin N.; Loxdale, H. D.; Heckel, D.; Weisser, 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.
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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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    Staff Profile: Dr. Franklin N. Nyabuga
    (2016-07) Nyabuga, Franklin N.
    Holds a PhD from Friedrich-Schiller University in Jena - Germany, a Master in Crop protection and Bachelor of Science (Agriculture Education and Extension) both from Egerton University, Njoro. For both Masters and PhD theses, I investigated various aspects of arthropod biology including population genetics, evolution, behavior and ecology. Also held two postdoctoral positions in Sweden at Lunds University and Swedish University of Agricultural Sciences - Alnarp, and researched on insect olfaction and communication, biodiversity and conservation.
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    Staff Profile: Franklin N. Nyabuga
    (2016-09) Nyabuga, Franklin N.
    Holds a PhD from Friedrich-Schiller University in Jena - Germany, a Master in Crop protection and Bachelor of Science (Agriculture Education and Extension) both from Egerton University, Njoro. For both Masters and PhD theses, I investigated various aspects of arthropod biology including population genetics, evolution, behavior and ecology. Also held two postdoctoral positions in Sweden at Lunds University and Swedish University of Agricultural Sciences - Alnarp, and researched on insect olfaction and communication, biodiversity and conservation.
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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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    Stay at home aphids: comparative spatial and seasonal metapopulation structure and dynamics of two specialist tansy aphid species studied using microsatellite markers
    (2011-06) Nyabuga, Franklin N.; Loxdale, H. D.; Weisser, W.; Heckel, David G.
    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.
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