The Association between Virus Prevalence and Intercolonial Aggression Levels in the Yellow Crazy Ant, Anoplolepis Gracilipes (Jerdon)

Hsu, Hung-Wei; Chiu, Ming‐Chung; Ching-Chen, Lee,; Lee, Chow‐Yang; Yang, Chun‐Pai

doi:10.3390/insects10120436

Cited by 11 publications

(13 citation statements)

References 39 publications

(48 reference statements)

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“…Evidence is emerging to suggest some of which can be pathogenic and associated with fitness cost of the host [ 63 ]. TR44839 virus was found to be highly prevalent in A. gracilipes populations in Okinawa (Japan), Taiwan, and Penang (Malaysia) [ 64 ], it, however, appears to persist in low viral titers (Hsu et al, unpublished data). The two dicistroviruses (Anoplolepis gracilipes virus 1 and Anoplolepis gracilipes virus 2) were also reported in the ant collected from Taiwan and Malaysia [ 62 ].…”

Section: Discussionmentioning

confidence: 99%

“…Gene flow between different supercolonies of A. gracilipes is limited because a high level of aggression is expected between workers (and possibly between worker and gyne) originating from different supercolonies, and this pattern applies even within a fine geographical scale [ 16 , 17 , 64 ]. Combined with the fact that independent foundation is rare in A .…”

Section: Discussionmentioning

confidence: 99%

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Ongoing Coevolution of Wolbachia and a Widespread Invasive Ant, Anoplolepis gracilipes

et al. 2020

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While Wolbachia are commonly found among arthropods, intraspecific infection rates can vary substantially across the geographic populations. Here we report nearly 100% prevalence of Wolbachia in the global populations of the yellow crazy ant, Anoplolepis gracilipes. To understand coevolutionary history between Wolbachia and A. gracilipes, we identified single nucleotide polymorphisms (SNPs) in Wolbachia from the ant across 12 geographical regions and compared the phylogeny of SNP-based Wolbachia to patterns of the ant’s mitochondrial DNA (mtDNA) variation. Our results revealed a strong concordance between phylogenies of Wolbachia and host mtDNA, providing immediate evidence of co-divergence. Among eight identified SNP loci separating the genetic clusters of Wolbachia, seven loci are located in potential protein-coding genes, three of which being non-synonymous SNPs that may influence gene functions. We found a Wolbachia hypothetical protein gene with signature of positive selection. These findings jointly allow us to characterize Wolbachia-ant coevolution and also raise a question about mechanism(s) underlying maintenance of high prevalence of Wolbachia during the colonization of this invasive ant.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Ongoing Coevolution of Wolbachia and a Widespread Invasive Ant, Anoplolepis gracilipes

et al. 2020

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“…DWV-positive ant colonies inhabiting in or nearby an apiary could be jump dispersed to somewhere distant from the apiary by the assistance of human transportation; (2) many invasive ant species form a unique social structure termed a “supercolony” in which physically separated nests are mutually tolerant to each other but aggressive to those belonging to a different supercolony. Such population structure has been shown to facilitate the horizontal transmission of pathogens among nests of invasive ants in an extensively large area due to the lack of visible nest boundaries that allows inter-nest interactions [ 39 ]. It would be interesting to test if DWV can be transmitted horizontally among ant nests within the same supercolony, especially given that DWV (and other honey bee viruses) is generally present at a low titer within ants [ 46 , 47 ].…”

Section: Discussionmentioning

confidence: 99%

“…Blasting the two primers with all available ant genomes in the Hymenoptera Genome Database [ 38 ] resulted in the absence of predicted amplification, further verifying specificity of the two primers. The cDNA was prepared from an additional worker from ant colonies previously confirmed to be positive for DWV ( Section 2.2 ) by PrimeScript TM 1st strand cDNA Synthesis Kit (Takara Bio Inc., Shiga, Japan) according to the manufacturer’s instructions, and used as a template for subsequent PCR amplification, following similar RT-PCR conditions and cycling profile as reported in Hsu et al [ 39 ]. Amplicons were confirmed by electrophoresis visualized on a UV transilluminator.…”

Section: Methodsmentioning

confidence: 99%

Deformed Wing Virus in Two Widespread Invasive Ants: Geographical Distribution, Prevalence, and Phylogeny

Lin

Lee

Nai

et al. 2020

Viruses

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Spillover of honey bee viruses have posed a significant threat to pollination services, triggering substantial effort in determining the host range of the viruses as an attempt to understand the transmission dynamics. Previous studies have reported infection of honey bee viruses in ants, raising the concern of ants serving as a reservoir host. Most of these studies, however, are restricted to a single, local ant population. We assessed the status (geographical distribution/prevalence/viral replication) and phylogenetic relationships of honey bee viruses in ants across the Asia–Pacific region, using deformed wing virus (DWV) and two widespread invasive ants, Paratrechina longicornis and Anoplolepis gracilipes, as the study system. DWV was detected in both ant species, with differential geographical distribution patterns and prevenance levels between them. These metrics, however, are consistent across the geographical range of the same ant species. Active replication was only evident in P. longicornis. We also showed that ant-associated DWV is genetically similar to that isolated from Asian populations of honey bees, suggesting that local acquisition of DWV by the invasive ants may have been common at least in some of our sampled regions. Transmission efficiency of DWV to local arthropods mediated by ant, however, may vary across ant species.

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“…2016). Hsu & al. (2019a) suggest that intercolonial aggressive behaviour in A. gracilipes was correlated with virus prevalence.…”

Section: Viral Infections That Change Ant Behaviourmentioning

confidence: 99%

Multi-host viruses in Argentine ants and honey bees: Increased viral disease in honey bees is associated with Argentine ants

Dobelmann¹

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Emerging infectious diseases threaten public health, livestock economies, and wildlife. Human-mediated species introductions can alter host and pathogen communities that shape the dynamics of infectious diseases. Several RNA viruses that have been linked to population declines in wild pollinators and losses of managed honey bees have been detected in multiple other species and are suspected to circulate within insect communities. Yet, we lack an understanding of how disease dynamics are affected by the introduction of novel species. These introduced species include invasive ants, which can disturb honey bees and become a pest in apiaries. The Argentine ant (Linepithema humile) is a globally successful invader that has been observed to attack bees and multiple bee-associated viruses have been detected in this ant species. Here, I studied interactions between Argentine ants and European honey bees (Apis mellifera) and how these interactions affect viral dynamics in beehives. I first tested a range of pollinators and associated insects for RNA viruses that are pathogenic to honey bees. Bee-associated viruses showed evidence for active viral replication in several pollinator species but also in species that cohabit in beehives such as ants, spiders, and cockroaches. Using phylogenetic analyses, I found that viral transmission within communities was shaped by geographic origin rather than being restricted by species barriers. Next, I used a longitudinal field study to test whether Argentine ant presence affected pathogen infections and survival in beehives. Argentine ants tested positive for three bee-associated viruses even before beehives were moved into ant-infested sites. Increased levels of deformed wing virus in beehives in autumn were associated with ant presence, although hive mortality was not affected by ants over the duration of this experiment. I used RNA sequencing on a subset of honey bee samples collected during autumn to study the RNA virome and identify transcriptomic responses associated with ant presence. Twelve RNA viruses were found in beehives, among those, three plant-associated viruses and an unclassified RNA virus that had not previously been observed in honey bees. Deformed wing virus showed the highest viral titres in most hives, but was only marginally affected by ant presence. Sacbrood virus and tomato ringspot virus levels were increased in hives with ants, however, both viruses are not known to infect Argentine ants and the plant-associated tomato ringspot virus seems unlikely to affect bee health. Lastly, I tested the feasibility of controlling Argentine ants in apiaries using a novel pest control strategy. RNA interference is a conserved cellular gene regulation mechanism that could be used to silence specific genes in ants. Using double-stranded RNA (dsRNA) to silence two immune-related genes in Argentine ants was expected to increase pathogen susceptibility, which could then lead to higher pathogen levels that reduce ant numbers. My results indicated that no consistent immune silencing could be achieved in the field. Immune gene expression changes were observed, but pathogen titres were not affected, and ant numbers stayed high. Argentine ant control using a conventional insecticide significantly increased bee survival, whereas many hives in the dsRNA and control group abandoned their hives due to ant attacks. Although population control was not successful using the two Argentine ant-specific dsRNAs, insights into ant immunity and ant-bee interactions could improve the development of novel control strategies. Bee-associated viruses have repeatedly been detected in ant species, yet, this is one of the first studies to investigate whether ants affect viral dynamics in honey bees. I showed that invasive Argentine ants are associated with increases in viral pathogens in honey bees. The mechanisms by which ants affect bee disease are unknown, although there is some evidence for ants transmitting viruses or causing stress responses in bees that affect immunity. The findings of this thesis highlight the risk of invasive ant species disrupting pollination services. New and environmentally-friendly methods to control invasive species are urgently needed to improve bee health and limit the spread of invasive ants, such as Argentine ants. The high prevalence of bee-associated viruses and viral diversity in ants suggests that pathogens that are suitable for population control might be present in ant populations, although risks of spillovers into other species need to be carefully considered.

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The Association between Virus Prevalence and Intercolonial Aggression Levels in the Yellow Crazy Ant, Anoplolepis Gracilipes (Jerdon)

Cited by 11 publications

References 39 publications

Ongoing Coevolution of Wolbachia and a Widespread Invasive Ant, Anoplolepis gracilipes

Ongoing Coevolution of Wolbachia and a Widespread Invasive Ant, Anoplolepis gracilipes

Deformed Wing Virus in Two Widespread Invasive Ants: Geographical Distribution, Prevalence, and Phylogeny

Multi-host viruses in Argentine ants and honey bees: Increased viral disease in honey bees is associated with Argentine ants

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