Effect of gregarines (Apicomplexa: Sporozoa) on survival and weight loss of Victorwithius similis (Arachnida: Pseudoscorpiones)

Bollatti, Fedra; Ceballos, Alejandra

doi:10.1016/j.jip.2014.01.002

Cited by 13 publications

(12 citation statements)

References 17 publications

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“…Although no gregarine species is currently known to be involved in this last type of relationship, the apparent benefits of gregarines on the survival of (starved) earwigs call for further experimental exploration of this hypothesis. Given the ubiquitous presence of gregarines among invertebrates (Bollatti and Ceballos, 2014;Criado-Fornelio et al, 2017), our data more generally suggest that this common member of the insect gut flora could have a positive yet currently neglected role in the life history of many host species (Harry, 1967;Hecker et al, 2002;Rodriguez et al, 2007).…”

Section: Discussionmentioning

confidence: 84%

“…Invertebrates typically host a great number of organisms in their gut, among which gregarines (Apicomplexa: Sporozoa) are probably the most frequently reported across terrestrial, marine and freshwater species (Bollatti and Ceballos, 2014;Criado-Fornelio et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…However, a few other works provide results that are at odds with those findings and show that the presence of gregarines can come with no costs or even provide apparent benefits for the host. For instance, a series of works demonstrate that gregarines do not shape growth, development time, adult size, resistance to starvation or adult survival in the water strider Gerris buenoi and the pseudoscorpion Victorwithius similis (Klingenberg et al, 1997;Bollatti and Ceballos, 2014). Conversely, the level of gregarine infection was positively associated with adult survival rates under food stress in the odonate Enallagma boreale (Hecker et al, 2002), with the speed of host development in the cat flea Ctenocephalides felis (Alarcón et al, 2017) and with the successful development of larvae under food stress in the mealworm beetle Tenebrio molitor (Harry, 1967;Rodriguez et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Friend or foe? The apparent benefits of gregarine (Apicomplexa: Sporozoa) infection in the European earwig

Arcila

Meunier

2020

International Journal for Parasitology

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Studying the costs and benefits of host-parasite interactions is of central importance to shed light on the evolutionary drivers of host life history traits. Although gregarines (Apicomplexa: Sporozoa) are one of the most frequent parasites in the gut of invertebrates, the diversity of its potential impacts on a host remains poorly explored. In this study, we addressed this gap in knowledge by investigating the prevalence of natural infections by the gregarine Gregarina ovata and testing how these infections shape a large set of morphological, behavioural and physiological traits in the European earwig Forficula auricularia. Our results first show that G. ovata was present in 76.8% of 573 field-sampled earwigs, and that its prevalence was both higher in males compared with females and increased between July and September. The load of G. ovata in the infected individuals was higher in males than females, but this sex difference vanished during the season. Our experiments then surprisingly revealed apparent benefits of G. ovata infections. Food-deprived hosts survived longer when they exhibited high compared with low gregarine loads. Moreover, the presence of gregarines was associated with a reduced phenoloxidase activity, indicating a lower immune resistance or a higher immune tolerance of the infected hosts. By contrast, we found no effect of G. ovata presence and number on earwigs' development (eye distance, forceps length), activity, food consumption or resistance against a fungal pathogen. Overall, our findings suggest that G. ovata could be involved in a mutualistic relationship with the European earwig. Given the ubiquitous presence of gregarines among invertebrates, our data also suggest that this common member of insect gut flora could have a broad and positive role in the life history of many host species.

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Section: Discussionmentioning

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Friend or foe? The apparent benefits of gregarine (Apicomplexa: Sporozoa) infection in the European earwig

Arcila

Meunier

2020

International Journal for Parasitology

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“…In addition, although many other apicomplexan protozoans are parasitic, such as Babesia, Theileria, and Cryptosporidium [ 56 ], Gregarina are highly diverse, ranging from parasitic to symbiotic [ 55 ]. There are reports of symbiotic Gregarina in arachnids [ 57 ], as well as in blood-sucking insects such as sand flies and mosquitoes [ 58 , 59 , 60 ]. Further studies are needed to determine the effects of tick-borne Gregarina on hosts, with the aim of devising new tick-control strategies.…”

Section: Discussionmentioning

confidence: 99%

Applications of Blocker Nucleic Acids and Non-Metazoan PCR Improves the Discovery of the Eukaryotic Microbiome in Ticks

et al. 2021

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Ticks serve as important vectors of a variety of pathogens. Recently, the viral and prokaryotic microbiomes in ticks have been explored using next-generation sequencing to understand the physiology of ticks and their interactions with pathogens. However, analyses of eukaryotic communities in ticks are limited, owing to the lack of suitable methods. In this study, we developed new methods to selectively amplify microeukaryote genes in tick-derived DNA by blocking the amplification of the 18S rRNA gene of ticks using artificial nucleic acids: peptide nucleic acids (PNAs) and locked nucleic acids (LNAs). In addition, another PCR using non-metazoan primers, referred to as UNonMet-PCR, was performed for comparison. We performed each PCR using tick-derived DNA and sequenced the amplicons using the Illumina MiSeq platform. Almost all sequences obtained by conventional PCR were derived from ticks, whereas the proportion of microeukaryotic reads and alpha diversity increased upon using the newly developed method. Additionally, the PNA- or LNA-based methods were suitable for paneukaryotic analyses, whereas the UNonMet-PCR method was particularly sensitive to fungi. The newly described methods enable analyses of the eukaryotic microbiome in ticks. We expect the application of these methods to improve our understanding of the tick microbiome.

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“…Sumner [36] suggested that gregarines are even essential for the growth of mealworm beetle larvae. Bollatti and Ceballos [37] showed that pseudoscorpions survived longer when they carried high gregarine loads, compared to the group with low gregarine loads, but overall, they suggested a commensalistic relationship. According to a study by Kaunisto et al [38], homozygous individuals of damselflies harboured more parasites, posing potentially strong selection pressure against inbreeding and homozygosity.…”

Section: What Is the Actual Life Strategy Of Gregarines?mentioning

confidence: 95%

The Symbiotic Spectrum: Where Do the Gregarines Fit?

Rueckert

Betts

Tsaousis

2019

Trends in Parasitology

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Gregarine apicomplexans are closely related to parasites such as Plasmodium, Toxoplasma, and Cryptosporidium, which are causing severe health and economic burdens. Colonizing only invertebrates and having no obvious medical relevance, they are mostly ignored in 'omics' studies, although gregarines are the most basal apicomplexans and therefore key players in the understanding of the evolution of parasitism in the Apicomplexa from free-living ancestors. They belong to the largest exclusively parasitic phylum, but is this perception actually true? The effects of gregarines on their hosts seem to cover the whole spectrum of symbiosis from mutualistic to parasitic. We suggest future research directions to understand the evolutionary role of gregarines, by elucidating their biology and interaction with their hosts and the hosts' microbiota. Parasitism in the Apicomplexa The phylum Apicomplexa contains unicellular parasites (currently more than 6000 named species) and is well known for its notorious pathogens of humans and livestock, such as Plasmodium (causative agent of malaria; mainly infecting humans, humanoids), Toxoplasma (toxoplasmosis; humans, cats), Eimeria (eimeriosis; poultry, cattle, ruminants), Theileria (theileriosis; cattle), Babesia (babesiosis; cattle, humans); Isospora (isosporiasis; humans), Cyclospora (cyclosporiasis; dogs, humans), and Cryptosporidium (cryptosporidiosis; humans, most livestock). These pathogens are of great public health concern and economic relevance, and they affect millions of people each year [1]. They all have intracellular life stages with the exception of Cryptosporidium [2], which has intracellular and extracytoplasmic stages [3,4]. Apicomplexans infect both invertebrates and vertebrates and have complex life cycles that differ considerably between the abovementioned groups [5] (Figure 1). Most of these life cycles involve at least two host species (i.e., a heteroxenous life cycle) (see Glossary). The apicomplexan clade is referred to in publications and textbooks as the largest phylum of eukaryotes that consists of obligate parasitic (Box 1) species only; but is this assumption really true for all apicomplexan species? The Gregarines Within the apicomplexans, gregarines are a unique subgroup that infects a wide range of freshwater, marine, and terrestrial invertebrates (almost exclusively). Different views concerning the taxonomy of the gregarines are emerging [6,7], but comprehensive evidence for a reliable overall taxonomic review is still missing. The latest review of eukaryotes still refers to the historic major groups Archigregarinorida, Eugregarinorida, and Neogregarinorida, mainly based on habitat, host range, and trophozoite morphology, to which is added the Cryptogregarinorida to accommodate Cryptosporidium [8] (Figure 1). Archigregarines are the most ancestral group, with a mix of ancestral and derived features, occurring in marine habitats only. Eugregarines can be found in marine, freshwater, and terrestrial habitats with large trophozoites that are morphologic...

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Effect of gregarines (Apicomplexa: Sporozoa) on survival and weight loss of Victorwithius similis (Arachnida: Pseudoscorpiones)

Cited by 13 publications

References 17 publications

Friend or foe? The apparent benefits of gregarine (Apicomplexa: Sporozoa) infection in the European earwig

Friend or foe? The apparent benefits of gregarine (Apicomplexa: Sporozoa) infection in the European earwig

Applications of Blocker Nucleic Acids and Non-Metazoan PCR Improves the Discovery of the Eukaryotic Microbiome in Ticks

The Symbiotic Spectrum: Where Do the Gregarines Fit?

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