Large-scale phylogeographic study of the cosmopolitan aphid pest<i>Brachycaudus helichrysi</i>reveals host plant associated lineages that evolved in allopatry

Popkin, Megan; Piffaretti, Joséphine; Clamens, Anne‐Laure; Qiao, Ge‐Xia; Chen, Jing; Vitalis, Renaud; Vanlerberghe‐Masutti, Flavie; Gupta, Rakesh Kumar; Lamaari, Malik; Langella, Olivier; d’Acier, Armelle Coeur; Jousselin, Emmanuelle

doi:10.1111/bij.12869

Cited by 12 publications

(26 citation statements)

References 61 publications

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“…Host-associated differentiation in M. dorsalis sp.2 parallels that seen in other insects (e.g., Frohlich, Torres-Jerez, Bedford, Markham, & Brown, 1999;Lozier et al, 2007;Popkin et al, 2017) and is more pronounced than the HAD seen in the classic example of Rhagoletis fruit flies and their parasitoids (which is apparent in nuclear allele frequencies, but not in mitochondrial haplotypes; Powell et al, 2013Powell et al, , 2014Hood et al, 2015). The rarity of gene flow between the two host races (identified in only seven of 112 individuals in our analyses) suggests that M. dorsalis sp.2 host races may be in the process of splitting into two daughter species, each specific to a single host oak section.…”

Section: Host-associated Structure and Speciation Within Megastigmussupporting

confidence: 59%

Partitioning of herbivore hosts across time and food plants promotes diversification in the Megastigmus dorsalis oak gall parasitoid complex

Nicholls

Schönrogge

Stone

2017

Ecology and Evolution

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Communities of insect herbivores and their natural enemies are rich and ecologically crucial components of terrestrial biodiversity. Understanding the processes that promote their origin and maintenance is thus of considerable interest. One major proposed mechanism is ecological speciation through host‐associated differentiation (HAD), the divergence of a polyphagous species first into ecological host races and eventually into more specialized daughter species. The rich chalcid parasitoid communities attacking cynipid oak gall wasp hosts are structured by multiple host traits, including food plant taxon, host gall phenology, and gall structure. Here, we ask whether the same traits structure genetic diversity within supposedly generalist parasitoid morphospecies. We use mitochondrial DNA sequences and microsatellite genotypes to quantify HAD for Megastigmus (Bootanomyia) dorsalis, a complex of two apparently generalist cryptic parasitoid species attacking oak galls. Ancient Balkan refugial populations showed phenological separation between the cryptic species, one primarily attacking spring galls, and the other mainly attacking autumn galls. The spring species also contained host races specializing on galls developing on different host‐plant lineages (sections Cerris vs. Quercus) within the oak genus Quercus. These results indicate more significant host‐associated structuring within oak gall parasitoid communities than previously thought and support ecological theory predicting the evolution of specialist lineages within generalist parasitoids. In contrast, UK populations of the autumn cryptic species associated with both native and recently invading oak gall wasps showed no evidence of population differentiation, implying rapid recruitment of native parasitoid populations onto invading hosts, and hence potential for natural biological control. This is of significance given recent rapid range expansion of the economically damaging chestnut gall wasp, Dryocosmus kuriphilus, in Europe.

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Section: Host-associated Structure and Speciation Within Megastigmussupporting

confidence: 59%

Partitioning of herbivore hosts across time and food plants promotes diversification in the Megastigmus dorsalis oak gall parasitoid complex

Nicholls

Schönrogge

Stone

2017

Ecology and Evolution

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“…The host plant range of B. helichrysi includes members of the Asteraceae, e.g. Chrysanthemum, species of Prunus and also species of Solanum, Fragaria, Trifolium, Medicago, Citrus and maize, Zea mays (Tatchell et al, 1983;Powell et al, 1992;Isac et al, 1998;Popkin et al, 2017). Viruses transmitted by this aphid include Plum Pox virus, Potato virus Y and Beet mild yellowing virus (Isac et al, 1998).…”

Section: High-input Conventionally Managed Fields (Hif)mentioning

confidence: 99%

Local Aphid Species Infestation on Invasive Weeds Affects Virus Infection of Nearest Crops Under Different Management Systems – A Preliminary Study

et al. 2020

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In the present study, we conducted field surveys to detect the population density of the most important invasive weed species and their associated virus vectoring aphids in crops grown under high input field (HIF) vs. low-input field (LIF) conditions, with and without fertilizers and pesticides. The most frequent invasive weed species were annual fleabane, Erigeron annua (L.), Canadian horseweed, Erigeron canadensis (L.) and Canadian goldenrod, Solidago canadensis (L.). These species were predominantly hosts of the aphids Brachycaudus helichrysi and Aulacorthum solani under both management systems. The 13% higher coverage of E. annua under LIF conditions resulted in a 30% higher B. helichrysi abundance and ∼85% higher A. solani abundance compared with HIF conditions. To reveal the incidence of virus infection in crop plants and invasive weeds, high-throughput sequencing of small RNAs was performed. Bioinformatics analysis combined with independent validation methods revealed the presence of six viruses, but with strikingly different patterns under LIF and HIF conditions. Their presence without symptoms in invasive weeds and crop plants supports the necessity of employing new approaches to those currently employed in invasive weed management. These findings also suggest that invasive weeds could serve as hosts for local aphid species and reservoirs for plant pathogenic viruses, both under low and high input management systems. In this light, as here demonstrated, viruses transmitted by local aphid species were found to differ between the management systems; hence, the importance of B. helichrysi and A. solani as virus vectors in particular clearly needs to be re-evaluated. Altogether, we accept that the present study is a pilot one and individual virus vectoring of aphids still needs to be directly tested. Even so, it represents one of the first contributions to this particular area, and thereby paves the way for further similar applied research in the future.

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“…From this standpoint, the effect of the virus vectoring aphids, whose host range naturally includes both local and invasive plant species from the same family (e.g. Asteraceae), needs to be considered in testing associational relations in plantplant interactions (Bell 1983;Popkin et al 2017).…”

Section: Low and High Input Agricultural Fields Have Different Effectmentioning

confidence: 99%

“…The host plant range of B. helichrysi includes members of the Asteraceae, e.g. Chrysanthemum, species of Prunus and also species of Solanum, Fragaria, Trifolium, Medicago, and Citrus and maize (Tatchell et al 1983;Powell et al 1992;Isac et al 1998;Popkin et al 2017). Viruses transmitted by these aphids include plum pox, Potato virus Y and the Beet mild yellowing virus (Isac et al 1998).…”

Section: Study Area Focal Weed and Aphid Speciesmentioning

confidence: 99%

Low and high input agricultural fields have different effects on pest aphid abundance via different invasive alien weed species

Kiss¹,

Bálint²,

Kőszeghi³

et al. 2019

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We conducted field surveys to detect the population density of the most important invasive weed species and their associated virus vectoring aphids in crops grown under high input field (HIF) vs low-input field (LIF) conditions, with and without fertilizers and pesticides. The most frequent invasive weed species were Stenactisannua, Erigeroncanadensis and Solidagocanadensis. These species were hosts predominantly for the aphids Brachycaudushelichrysi and Aulacorthumsolani in both management systems. The 13% higher coverage of S.annua under LIF conditions resulted in a 30% higher B.helichrysi abundance and ~85% higher A.solani abundance compared with HIF conditions. Host plant quality was assessed by measuring peroxidase enzyme activity. There was a significantly increased POD activity at 10 μmol min−1 mg protein−1 unit in S.annua under LIF conditions, suggesting a higher stress by aphids under this management regime. The high colonization intensity of B.helichrysi on maize, potato and alfalfa crops were detected from both S.annua and E.canadensis. We conclude that new and faster methods need to be used to prevent colonization of such virus vectoring aphids and their host plants, even under low input regimes.

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Large-scale phylogeographic study of the cosmopolitan aphid pestBrachycaudus helichrysireveals host plant associated lineages that evolved in allopatry

Cited by 12 publications

References 61 publications

Partitioning of herbivore hosts across time and food plants promotes diversification in the Megastigmus dorsalis oak gall parasitoid complex

Partitioning of herbivore hosts across time and food plants promotes diversification in the Megastigmus dorsalis oak gall parasitoid complex

Local Aphid Species Infestation on Invasive Weeds Affects Virus Infection of Nearest Crops Under Different Management Systems – A Preliminary Study

Low and high input agricultural fields have different effects on pest aphid abundance via different invasive alien weed species

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