Ecological characteristics of insects that affect symbiotic relationships with mites

Parasites and pathogens that begin as symbionts, i.e., organisms living together in the same habitat, are some of the most promising drivers of species evolution. Because insects are highly diverse and important as ecosystem service agents and because mites can exert large effects on insect populations (capable of killing at least juveniles), insect–mite interactions have been analyzed from various perspectives, including evolutionary, ecological and pest‐management perspectives. Here, I review and examine insect–mite symbiotic associations to develop hypotheses concerning the factors that maintain and develop their relationships. Previous studies have hypothesized that insect sociality and mite richness and specificity affect insect–mite interactions. I found that both solitary and social insects, including parasocial and subsocial insects, harbor numbers of symbionts including species‐specific ones but few dangerous mite symbionts in their nests or habitats under natural conditions. Nest size or the amount of food resources in a nest may affect mite richness. On the basis of this review, I hypothesize that the insect characteristics relevant for mite symbiotic hosting are sharing the same habitat with mites and living in a nutrient‐rich habitat. I also suggest that many cases of species‐specific symbiosis began with phoresy. To test these hypotheses, phylogenetic information on mites living with insect groups and quantitative analysis to characterize each insect–mite relationship are necessary.     

昆虫共生微生物在病虫害和疾病控制上的应用前景

昆虫与微生物之间的互利共生关系是自然界中一种常见的互作形式。昆虫的种类丰富多样并且在自然界中分布广泛,在一定程度上得益于共生微生物的帮助。随着生物技术的不断发展,越来越多的共生微生物和互利共生模式得以发现并深入研究。微生物不仅能够为昆虫的生长发育提供营养,还能合成很多生物活性物质、调节宿主的免疫、对抗捕食者和抵御病原微生物感染,成为宿主昆虫健康和适应的守护者。鉴于共生微生物与昆虫生理生态的密切联系,以及昆虫对人类经济与健康的重要影响,利用共生微生物对昆虫及虫媒病进行生物控制已经成为一个热点研究方向,并展现了良好的应用前景。本文对昆虫共生微生物的多样性、生物学功能、与宿主相互作用机制及其在病虫害和虫媒病防治中的研究进展进行综述和展望。     

Intraspecific phylogenetic congruence among multiple symbiont genomes

Eukaryotes often form intimate endosymbioses with prokaryotic organisms. Cases in which these symbionts are transmitted cytoplasmically to host progeny create the potential for co-speciation or congruent evolution among the distinct genomes of these partners. If symbionts do not move horizontally between different eukaryotic hosts, strict phylogenetic congruence of their genomes is predicted and should extend to relationships within a single host species. Conversely, even rare 'host shifts' among closely related lineages should yield conflicting tree topologies at the intraspecific level. Here, we investigate the historical associations among four symbiotic genomes residing within an aphid host: the mitochondrial DNA of Uroleucon ambrosiae aphids, the bacterial chromosome of their Buchnera bacterial endosymbionts, and two plasmids associated with Buchnera. DNA sequence polymorphisms provided a significant phylogenetic signal and no homoplasy for each data set, yielding completely and significantly congruent phylogenies for these four genomes and no evidence of horizontal transmission. This study thus provides the first evidence for strictly vertical transmission and 'co-speciation' of symbiotic organisms at the intraspecific level, and represents the lowest phylogenetic level at which such coevolution has been demonstrated. These results may reflect the obligate nature of this intimate mutualism and indicate opportunities for adaptive coevolution among linked symbiont genomes.     

Virulence and transmission of infectious diseases in humans and insects: evolutionary and demographic patterns

The rate and degree of proliferation of disease organisms determine their pathogenicity and the efficiency of their transmission. These traits dictate the impact of a disease on individuals as well as populations. Virulence and transmission of diseases are molded by evolutionary forces - pathogens and hosts are each selected to reproduce and persist. New ideas about the evolution of human diseases also apply to the relationships between insects and their diseases. Evidence for close associations between insects and pathogens include the viral suppression of insect molting hormones and the occurrence of latent virus that can be activated by foreign viruses.     

Novel strategies targeting pathogen transmission reduction in insect vectors: Tsetse-transmitted trypanosomiasis control

Insect vectors are essential for the transmission of important human diseases such as malaria, leishmaniasis, Chagas and sleeping sickness. Insects are also responsible for the transmission of agricultural diseases that affect livestock and crops. Traditionally, control of the vector populations has been an effective disease management strategy. Recently, vector control strategies have been fortified by research in insect biology and in insect–pathogen interactions as well as by the development of transgenic technologies. In addition to insect population reduction methods, disease control via selective elimination of pathogens in insects can now be explored. Here we explore the tsetse vectors of African trypanosomes and describe the application of recent knowledge gained in their symbiotic, reproductive and vectorial biology to develop novel disease control strategies.     

共生微生物对昆虫化学感受的影响北大核心

共生微生物通过影响昆虫信息化合物的合成或感受来调控宿主的化学通讯,进而影响昆虫的交流、防御、捕食和扩散行为。这种调控作用有助于共生微生物的扩散,但对宿主可能是有利的,也可能是有害的,并为共生体系的协同进化提供动力。本文围绕近年来共生微生物对昆虫化学感受的影响及其机制展开综述,并分析其进化意义,旨在为昆虫化学生态学理论提供补充,并为开发新的害虫防治策略提供思路。     

A perspective on insect–microbe holobionts facing thermal fluctuations in a climate-change context

Temperature influences the ecology and evolution of insects and their symbionts by impacting each partner independently and their interactions, considering the holobiont as a primary unit of selection. There are sound data about the responses of these partnerships to constant temperatures and sporadic thermal stress (mostly heat shock). However, the current understanding of the thermal ecology of insect–microbe holobionts remains patchy because the complex thermal fluctuations (at different spatial and temporal scales) experienced by these organisms in nature have often been overlooked experimentally. This may drastically constrain our ability to predict the fate of mutualistic interactions under climate change, which will alter both mean temperatures and thermal variability. Here, we tackle down these issues by focusing on the effects of temperature fluctuations on the evolutionary ecology of insect–microbe holobionts. We propose potentially worth-investigating research avenues to (i) evaluate the relevance of theoretical concepts used to predict the biological impacts of temperature fluctuations when applied to holobionts; (ii) acknowledge the plastic (behavioural thermoregulation, physiological acclimation) and genetic responses (evolution) expressed by holobionts in fluctuating thermal environments; and (iii) explore the potential impacts of previously unconsidered patterns of temperature fluctuations on the outcomes and the dynamic of these insect–microbe associations.     

The natural occurrence of secondary bacterial symbionts in aphids

1. Many insects host secondary bacterial symbionts that are known to have wide‐ranging effects on their hosts, from host‐plant use to resistance against natural enemies. This has been most widely studied in aphids, which have become a model system to study insect–bacteria interactions. 2. While there is an increasing understanding of the role of symbionts in aphids from controlled laboratory studies, we are only beginning to explore the impact of hosting these symbionts on eco‐evolutionary dynamics in natural systems. To date, many research groups have identified bacterial symbionts from various aphid species, providing us with a bank of literature on aphid–symbiont associations in natural populations. 3. The role of secondary symbionts in aphids is discussed, and the taxonomic and geographical distribution of symbionts among aphids are summarised, and the potential reasons for the patterns observed. The need to test for multiple symbiont species (and co‐infections) across many individuals and the whole distribution range of an aphid is highlighted, including sampling on all known host‐plant species. 4. It is further important also to consider variation within the symbiont, the aphid‐host and the surrounding community, e.g. host‐plants or the natural enemies, to understand how these have the potential to mediate aphid–symbiont interactions. 5. Finally, the knowledge gained from experimental work should now be used to understand the role of aphid secondary symbionts in field systems, to fully understand the potentially far‐reaching consequences of aphid endosymbionts on community and ecosystem processes.     

Co-niche construction between hosts and symbionts: ideas and evidence

Symbiosis is a process that can generate evolutionary novelties and can extend the phenotypic niche space of organisms. Symbionts can act together with their hosts to co-construct host organs, within which symbionts are housed. Once established within hosts, symbionts can also influence various aspects of host phenotype, such as resource acquisition, protection from predation by acquisition of toxicity, as well as behaviour. Once symbiosis is established, its fidelity between generations must be ensured. Hosts evolve various mechanisms to screen unwanted symbionts and to facilitate faithful transmission of mutualistic partners between generations. Microbes are the most important symbionts that have influenced plant and animal phenotypes; multicellular organisms engage in developmental symbioses with microbes at many stages in ontogeny. The co-construction of niches may result in composite organisms that are physically nested within each other. While it has been advocated that these composite organisms need new evolutionary theories and perspectives to describe their properties and evolutionary trajectories, it appears that standard evolutionary theories are adequate to explore selection pressures on their composite or individual traits. Recent advances in our understanding of composite organisms open up many important questions regarding the stability and transmission of these units.     

Cospeciation in the triplex symbiosis of termite gut protists (Pseudotrichonympha spp.), their hosts, and their bacterial endosymbionts

A number of cophylogenetic relationships between two organisms namely a host and a symbiont or parasite have been studied to date; however, organismal interactions in nature usually involve multiple members. Here, we investigated the cospeciation of a triplex symbiotic system comprising a hierarchy of three organisms -- termites of the family Rhinotermitidae, cellulolytic protists of the genus Pseudotrichonympha in the guts of these termites, and intracellular bacterial symbionts of the protists. The molecular phylogeny was inferred based on two mitochondrial genes for the termites and nuclear small-subunit rRNA genes for the protists and their endosymbionts, and these were compared. Although intestinal microorganisms are generally considered to have looser associations with the host than intracellular symbionts, the Pseudotrichonympha protists showed almost complete codivergence with the host termites, probably due to strict transmissions by proctodeal trophallaxis or coprophagy based on the social behaviour of the termites. Except for one case, the endosymbiotic bacteria of the protists formed a monophyletic lineage in the order Bacteroidales, and the branching pattern was almost identical to those of the protists and the termites. However, some non-codivergent evolutionary events were evident. The members of this triplex symbiotic system appear to have cospeciated during their evolution with minor exceptions; the evolutionary relationships were probably established by termite sociality and the complex microbial community in the gut.     

Dynamics of multiple symbiont density regulation during host development: tsetse fly and its microbial flora

Symbiotic associations often enhance hosts' physiological capabilities, allowing them to expand into restricted terrains, thus leading to biological diversification. Stable maintenance of partners is essential for the overall biological system to succeed. The viviparous tsetse fly (Diptera: Glossinidae) offers an exceptional system to examine factors that influence the maintenance of multiple symbiotic organisms within a single eukaryotic host. This insect harbours three different symbionts representing diverse associations, coevolutionary histories and transmission modes. The enterics, obligate mutualist Wigglesworthia and beneficial Sodalis, are maternally transmitted to the intrauterine larvae, while parasitic Wolbachia infects the developing oocyte. In this study, the population dynamics of these three symbionts were examined through host development and during potentially disruptive events, including host immune challenge, the presence of third parties (such as African trypanosomes) and environmental perturbations (such as fluctuating humidity levels). While mutualistic partners exhibited well-regulated density profiles over different host developmental stages, parasitic Wolbachia infections varied in individual hosts. Host immune status and the presence of trypanosome infections did not impact the steady-state density levels observed for mutualistic microbes in either sex, while these factors resulted in an increase in Wolbachia density in males. Interestingly, perturbation of the maternal environment resulted in the deposition of progeny harbouring greater overall symbiont loads. The regulation of symbiont density, arising from coadaptive processes, may be an important mechanism driving inter-specific relations to ensure their competitive survival and to promote specialization of beneficial associations.     

Mosquito symbioses: from basic research to the paratransgenic control of mosquito‐borne diseases

Mosquito‐borne diseases pose significant concerns in public health. Microbial symbionts of mosquitoes are attracting quite a lot of interest in relation to the development of novel strategies aimed to reduce mosquito vectorial capacity with particular regard to paratransgenesis that relies on genetically modified mosquito symbionts to express molecules within the vector able to interfere with parasite development and transmission. Here, we review the present status of the knowledge of mosquito–symbionts relationships, focusing on perspective in the application of symbiotic control in developing an efficient management of mosquito‐borne diseases.     

按蚊肠道微生物及其在阻断疟疾传播上的应用

按蚊体内,尤其是中肠内定殖着大量的微生物群落。肠道菌群通过与按蚊的长期协同进化形成了相互依存的共生关系。肠道共生菌参与调节按蚊的多种生命活动,对于维持按蚊的健康发挥着重要作用,已经成为一个与宿主按蚊密不可分的重要"器官"。研究表明,肠道共生菌在按蚊物质代谢、营养、发育、生殖、免疫调控和免疫防御等生理过程中发挥着重要的调节作用。蚊虫是疟疾、登革、寨卡等多种疾病的传播媒介,而肠道共生菌对寄生虫和病毒在蚊虫肠道内的发育和感染具有重要影响,因此研究蚊虫与共生菌的相互作用有着重要的理论和实践意义。本文将对按蚊肠道共生菌的多样性、生物学功能、与宿主相互作用的机制及其在防治疟疾上的应用进展进行综述,并对未来的研究提出展望。     

Slow algae, fast fungi: exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa

Omphalina basidiolichens are obligate mutualistic associations of a fungus of the genus Omphalina (the exhabitant) and a unicellular green alga of the genus Coccomyxa (the inhabitant). It has been suggested that symbiotic inhabitants have a lower rate of genetic change compared to exhabitants because the latter are more exposed to abiotic environmental variation and competition from other organisms. In order to test this hypothesis we compared substitution rates in the nuclear ribosomal internal transcribed spacer region (ITS1, 5.8S, ITS2) among fungal species with rates among their respective algal symbionts. To ensure valid comparisons, only taxon pairs (12) with a common evolutionary history were used. On average, substitution rates in the ITS1 portion of Omphalina pairs were 27.5 times higher than rates in the corresponding pairs of Coccomyxa since divergence from their respective ancestor at the base of the Omphalina/Coccomyxa lineage. Substitution rates in the 5.8S and the ITS2 portions were 2.4 and 18.0 times higher, respectively. The highest rate difference (43.0) was found in the ITS1 region. These are, to our knowledge, the highest differences of substitution rates reported for symbiotic organisms. We conclude that the Omphalina model system conforms to the proposed hypothesis of lower substitution rates in the inhabitant, but that the mode of transmission of the inhabitant (vertical versus horizontal) could be a prevailing factor in the regulation of unequal rates of nucleotide substitution between co-evolving symbionts. Our phylogenetic study of Coccomyxa revealed three main lineages within this genus, corresponding to free-living Coccomyxa, individuals isolated from basidiolichens Omphalina and Coccomyxa isolated from ascolichens belonging to the Peltigerales.     

Incorporating the process of vertical transmission into understanding of host–symbiont dynamics

Variation exists in the frequency of obligate, vertically transmitted symbiotic organisms within and among host populations; however, these patterns have not been adequately explained by variable fitness effects of symbionts on their hosts. In this forum, we call attention to another equally important, but overlooked mechanism to maintain variation in the frequency of symbioses in nature: the rate of vertical transmission. On ecological time scales, vertical transmission can affect the equilibrium frequencies of symbionts in host populations, with potential consequences for population and community dynamics. In addition, vertical transmission has the potential to influence the evolution of symbiosis, by affecting the probability of fixation of symbiosis (and therefore the evolution of complexity) and by allowing hosts to sanction against costly symbionts. Here we use grass–epichloae symbioses as a model system to explore the causes and consequences of variation in vertical transmission rates. We identify critical points for symbiont transmission that emerge from considering the host growth cycle devoted to reproduction (asexual vs sexual) and the host capability to maintain homeostasis. We also use information on the process of transmission to predict the environmental factors that would most likely affect transmission rates. Altogether, we aim to highlight the vertical transmission rate as an important process for understanding the ecology and evolution of symbiosis, using grass–epichloae interactions as a case study.     

Betaproteobacterial symbionts of the ciliate Euplotes: origin and tangled evolutionary path of an obligate microbial association

The Polynucleobacter-Euplotes association is an obligatory symbiotic system between a monophyletic group of ciliate species belonging to the genus Euplotes and bacteria of the species Polynucleobacter necessarius (Betaproteobacteria). Both organisms are unable to survive independently. Several studies revealed the existence of free-living populations of Polynucleobacter bacteria which are phylogenetically closely related to the endosymbiotic ones, but never share associations with Euplotes in the natural environment. Hence, following the most parsimonious explanation on the origin of the association, this symbiosis should represent a synapomorphic character for the hosts' clade. Nevertheless, phylogenetic analyses performed on an increased number of strains here presented suggest that Euplotes species, during their evolution, recruited Polynucleobacter bacteria as symbionts more than once. Moreover, in three cases, we observed different bacteria as obligate symbionts. These symbionts are the first characterized representatives of a phylogenetic lineage branching in a basal position with respect to the genus Polynucleobacter. The hypothesis that the original obligate symbionts belonged to this newly discovered clade and that, only subsequently, in most cases they have been replaced by Polynucleobacter bacteria recruited from the environment is proposed and discussed. The evolutionary path of this association seems anyway to have been more complex than so far supposed.     

How many symbionts are provided by mothers,acquired by offspring,and needed for successful vertical transmission in an obligate insect–bacterium mutualism?

Vertical symbiont transmission is among the most pivotal processes for maintenance of symbiotic associations. However, it is poorly understood whether and how the levels of resource allocation and investment upon vertical transmission are regulated. The stinkbug Megacopta punctatissima is obligatorily associated with the gut symbiotic bacterium 'Candidatus Ishikawaella capsulata', whose transmission is mediated by a unique mechanism called 'symbiont capsule'. We investigated the population dynamics of the symbiont during vertical transmission in the host-symbiont mutualism. The stinkbug mothers produced one capsule for around 3.6 eggs irrespective of clutch size, suggesting a strict maternal control over symbiont supply for the offspring. However, experimental manipulation of egg/capsule ratios revealed that one capsule is sufficient for symbiont transmission to six nymphs. Quantitative polymerase chain reaction analyses demonstrated that a capsule contains 1.2 x 10(8) symbionts, a newborn nymph possesses 2 x 10(7) symbionts from a capsule, and thus one capsule certainly contains a sufficient amount of symbiont cells for six nymphs. These results indicated that the stinkbug mothers produce 1.7 times more symbiont capsules than needed. The newborn nymphs consistently harboured around 2 x 10(7) symbionts, also suggesting a nymphal control over symbiont transmission. The threshold symbiont titre minimally needed for successful vertical transmission was estimated to be 1.9 x 10(6) symbionts, which is only 1/10 of the actual symbiont titre detected in a newborn nymph. These results illuminate several ecological factors that may be relevant to parental and offspring controls over symbiotic resource allocation through host insect generations.     

Droplet digital PCR as a tool for investigating dynamics of cryptic symbionts

Interactions among symbiotic organisms and their hosts are major drivers of ecological and evolutionary processes. Monitoring the infection patterns among natural populations and identifying factors affecting these interactions are critical for understanding symbiont–host relationships. However, many of these interactions remain understudied since the knowledge about the symbiont species is lacking, which hinders the development of appropriate tools. In this study, we developed a digital droplet PCR (ddPCR) assay based on apicomplexan COX1 gene to detect an undescribed agamococcidian symbiont. We show that the method gives precise and reproducible results and enables detecting cryptic symbionts in low target concentration. We further exemplify the assay''s use to survey seasonally sampled natural host (Pygospio elegans) populations for symbiont infection dynamics. We found that symbiont prevalence differs spatially but does not show seasonal changes. Infection load differed between populations and was low in spring and significantly increased towards fall in all populations. We also found that the symbiont prevalence is affected by host length and population density. Larger hosts were more likely to be infected, and high host densities were found to have a lower probability of infection. The observed variations could be due to characteristics of both symbiont and host biology, especially the seasonal variation in encounter rates. Our findings show that the developed ddPCR assay is a robust tool for detecting undescribed symbionts that are otherwise difficult to quantify, enabling further insight into the impact cryptic symbionts have on their hosts.     

The Bacteriome of Bat Flies (Nycteribiidae) from the Malagasy Region: a Community Shaped by Host Ecology,Bacterial Transmission Mode,and Host-Vector Specificity

The Nycteribiidae are obligate blood-sucking Diptera (Hippoboscoidea) flies that parasitize bats. Depending on species, these wingless flies exhibit either high specialism or generalism toward their hosts, which may in turn have important consequences in terms of their associated microbial community structure. Bats have been hypothesized to be reservoirs of numerous infectious agents, some of which have recently emerged in human populations. Thus, bat flies may be important in the epidemiology and transmission of some of these bat-borne infectious diseases, acting either directly as arthropod vectors or indirectly by shaping pathogen communities among bat populations. In addition, bat flies commonly have associations with heritable bacterial endosymbionts that inhabit insect cells and depend on maternal transmission through egg cytoplasm to ensure their transmission. Some of these heritable bacteria are likely obligate mutualists required to support bat fly development, but others are facultative symbionts with unknown effects. Here, we present bacterial community profiles that were obtained from seven bat fly species, representing five genera, parasitizing bats from the Malagasy region. The observed bacterial diversity includes Rickettsia, Wolbachia, and several Arsenophonus-like organisms, as well as other members of the Enterobacteriales and a widespread association of Bartonella bacteria from bat flies of all five genera. Using the well-described host specificity of these flies and data on community structure from selected bacterial taxa with either vertical or horizontal transmission, we show that host/vector specificity and transmission mode are important drivers of bacterial community structure.     

Different mosquito species host Wickerhamomyces anomalus (Pichia anomala): perspectives on vector-borne diseases symbiotic control

The genetic manipulation of the microbial community associated with hematophagus insects is particularly relevant for public health applications. Within mosquito populations, this relationship has been overlooked until recently. New advances in molecular biotechnology propose the genetic manipulation of mosquito symbionts to prevent the transmission of pathogens to humans by interfering with the obligatory life cycle stages within the insect through the use of effector molecules. This approach, defined as 'paratransgenesis', has opened the way for the investigation and characterization of microbes residing in the mosquito body, particularly those localised within the gut. Some interesting bacteria have been identified as candidates for genetic modification, however, endosymbiotic yeasts remain largely unexplored with little information on the symbiotic relationships to date. Here we review the recent report of symbiotic relationship between Wickerhamomyces anomalus (Pichia anomala) and several mosquito vector species as promising methods to implement control of mosquito-borne diseases.