The role of animal hosts in shaping gut microbiome variation.

Millions of years of co-evolution between animals and their associated microbial communities have shaped and diversified the nature of their relationship. Studies continue to reveal new layers of complexity in host-microbe interactions, the fate of which depends on a variety of different factors, ranging from neutral processes and environmental factors to local dynamics. Research is increasingly integrating ecosystem-based approaches, metagenomics and mathematical modelling to disentangle the individual contribution of ecological factors to microbiome evolution. Within this framework, host factors are known to be among the dominant drivers of microbiome composition in different animal species. However, the extent to which they shape microbiome assembly and evolution remains unclear. In this review, we summarize our understanding of how host factors drive microbial communities and how these dynamics are conserved and vary across taxa. We conclude by outlining key avenues for research and highlight the need for implementation of and key modifications to existing theory to fully capture the dynamics of host-associated microbiomes. This article is part of the theme issue 'Sculpting the microbiome: how host factors determine and respond to microbial colonization'.

Impact of herbivore symbionts on parasitoid foraging behaviour.

Parasitoids are insects that lay eggs in other insects, but before this, they have the remarkable task of locating and successfully attacking a suitable individual. Once an egg is laid, many herbivorous hosts carry defensive symbionts that prevent parasitoid development. Some symbioses can act ahead of these defences by reducing parasitoid foraging efficiency, while others may betray their hosts by producing chemical cues that attract parasitoids. In this review, we provide examples of symbionts altering the different steps that adult parasitoids need to take to achieve egg laying. We also discuss how interactions between habitat complexity, plants and herbivores modulate the way symbionts affect parasitoid foraging, and parasitoid evaluation of patch quality based on risk cues derived from parasitoid antagonists such as competing parasitoids and predators.

Joint species distributions reveal the combined effects of host plants, abiotic factors and species competition as drivers of species abundances in fruit flies.

The relative importance of ecological factors and species interactions for shaping species distributions is still debated. The realised niches of eight sympatric tephritid fruit flies were inferred from field abundance data using joint species distribution modelling and network inference, on the whole community and separately on three host plant groups. These estimates were then confronted the fundamental niches of seven fly species estimated through laboratory-measured fitnesses on host plants. Species abundances depended on host plants, followed by climatic factors, with a dose of competition between species sharing host plants. The relative importance of these factors mildly changed among the three host plant groups. Despite overlapping fundamental niches, specialists and generalists had almost distinct realised niches, with possible competitive exclusion of generalists by specialists on Cucurbitaceae. They had different assembly rules: Specialists were mainly influenced by their adaptation to host plants, while generalist abundances varied regardless of their fundamental host use.

Benefits and costs of hosting facultative symbionts in plant-sucking insects: A meta-analysis.

Many animals have evolved associations with symbiotic microbes that benefit the host through increased growth, lifespan, and survival. Some interactions are obligate (essential for survival) while others are facultative (usually beneficial but not essential). Not all individuals host all facultative symbionts in a population, and thus there is probably a trade-off between the cost of hosting these symbionts and the benefits they confer to the host. Plant-sucking insects have been one of the most important models to test these costs and benefits experimentally. This research is now moving beyond the description of symbiont effects towards understanding the mechanisms of action, and their role in the wider ecological community. We present a quantitative and systematic analysis of the published evidence exploring this question. We found that whitefly and true bugs experience benefits through increased growth and fecundity, whereas aphids experience costs to their fecundity but benefits through increased resistance to natural enemies. We also report the lack of data in some plant-sucking groups, and explore variation in effect strengths and directions across aphid host, symbiont and plant species thus highlighting the importance of considering the context dependency of these interactions.

A meta-analysis of biological impacts of artificial light at night.

Natural light cycles are being eroded over large areas of the globe by the direct emissions and sky brightening that result from sources of artificial night-time light. This is predicted to affect wild organisms, particularly because of the central role that light regimes play in determining the timing of biological activity. Although many empirical studies have reported such effects, these have focused on particular species or local communities and have thus been unable to provide a general evaluation of the overall frequency and strength of these impacts. Using a new database of published studies, we show that exposure to artificial light at night induces strong responses for physiological measures, daily activity patterns and life history traits. We found particularly strong responses with regards to hormone levels, the onset of daily activity in diurnal species and life history traits, such as the number of offspring, predation, cognition and seafinding (in turtles). So far, few studies have focused on the impact of artificial light at night on ecosystem functions. The breadth and often strength of biological impacts we reveal highlight the need for outdoor artificial night-time lighting to be limited to the places and forms-such as timing, intensity and spectrum-where it is genuinely required by the people using it to minimize ecological impacts.

Dendrothripoides moundi (Thysanoptera, Thripidae), a new species from Madagascar.

The genus Dendrothripoides was originally described by Bagnall (1923) from India and is currently represented by five species (ThripsWiki 2020). Dendrothripoides innoxius (Karny) is widely distributed in the Oriental and Pacific regions; D. microchaetus Okajima is from the Philippines and Indonesian archipelago; D. nakaharai Reyes known only from the Philippines, D. poni Kudo from Thailand, and D. venustus Faure from Rhodesia [Zimbabwe] and South Africa (Faure 1941; Kudo 1977; Bournier 2000). Little is known about the biology of these species because collections often have samples with few specimens. D. innoxius is considered a minor pest on Ipomoea crops (Watson Mound 2020) but adults have been taken on the leaves of plants in numerous families (Asteraceae, Convolvulaceae, Dioscoreaceae, Musaceae, Poaceae). Dendrothripoides was classified within the Panchaetothripinae by Priesner (1957) for having a reticulate body surface. However, Ananthakrishnan (1963) indicated that the similarities are superficial, and that this genus should be classified in the Aptinothripina of the Thripinae because the pronotum lacks long setae. The genus is now not included in the Anaphothrips genus-group (Masumoto Okajima 2017), but the systematic position is unclear with a recent morphological phylogenetic analysis indicating a position near the Panchaetothripinae that may be due to superficial resemblance (Zhang et al. 2019).

A new species of the genus Thrips (Thysanoptera, Thripidae) from the Malagasy Region.

The genus Thrips comprises 296 species (ThripsWiki 2019) and is the largest of all Terebrantian genera. The only other Thysanopteran genera comparable in size are the phlaeothripids Haplothrips and Liothrips. Species of Thrips can be found in flowers and on leaves of a wide variety of plants from grasses to trees. Most of them are beneficial pollinators (Garcia-Fayos Goldarazena 2008; Eliyahu et al. 2015), while others are pests and cause significant economic damage (Mound Marullo 1996). Some of them are polyphagous and widespread, while others are rarely seen and restricted to one species of plant (Palmer 1992).

Impact of host endosymbionts on parasitoid host range - from mechanisms to communities.

In insects, bacterial endosymbionts are known to influence the ecology of their hosts by modifying interactions with natural enemies such as parasitoids. Symbionts can modulate both parasitoid behavioral and/or physiological traits as well as host behaviors and life-history traits. Together these suggest that endosymbionts may impact the host range of parasitoids. For example, endosymbionts may narrow parasitoid host range through first, reducing parasitoid ability to locate hosts and/or larval survival, second, affecting fitness traits of the emerging adult parasitoid and/or third, modulating the outcome of interference and exploitative competition between parasitoid species. From both a fundamental and applied point of view, these symbiotic effects would influence the ecology and evolution of parasitoids and associated population-level processes and ecosystem services (e.g. biocontrol).

Bacterial Symbionts in Lepidoptera: Their Diversity, Transmission, and Impact on the Host.

The insect's microbiota is well acknowledged as a "hidden" player influencing essential insect traits. The gut microbiome of butterflies and moths (Lepidoptera) has been shown to be highly variable between and within species, resulting in a controversy on the functional relevance of gut microbes in this insect order. Here, we aim to (i) review current knowledge on the composition of gut microbial communities across Lepidoptera and (ii) elucidate the drivers of the variability in the lepidopteran gut microbiome and provide an overview on (iii) routes of transfer and (iv) the putative functions of microbes in Lepidoptera. To find out whether Lepidopterans possess a core gut microbiome, we compared studies of the microbiome from 30 lepidopteran species. Gut bacteria of the Enterobacteriaceae, Bacillaceae, and Pseudomonadaceae families were the most widespread across species, with Pseudomonas, Bacillus, Staphylococcus, Enterobacter, and Enterococcus being the most common genera. Several studies indicate that habitat, food plant, and age of the host insect can greatly impact the gut microbiome, which contributes to digestion, detoxification, or defense against natural enemies. We mainly focus on the gut microbiome, but we also include some examples of intracellular endosymbionts. These symbionts are present across a broad range of insect taxa and are known to exert different effects on their host, mostly including nutrition and reproductive manipulation. Only two intracellular bacteria genera (Wolbachia and Spiroplasma) have been reported to colonize reproductive tissues of Lepidoptera, affecting their host's reproduction. We explore routes of transmission of both gut microbiota and intracellular symbionts and have found that these microbes may be horizontally transmitted through the host plant, but also vertically via the egg stage. More detailed knowledge about the functions and plasticity of the microbiome in Lepidoptera may provide novel leads for the control of lepidopteran pest species.

Symbionts protect aphids from parasitic wasps by attenuating herbivore-induced plant volatiles.

Plants respond to insect attack by releasing blends of volatile chemicals that attract their herbivores' specific natural enemies, while insect herbivores may carry endosymbiotic microorganisms that directly improve herbivore survival after natural enemy attack. Here we demonstrate that the two phenomena can be linked. Plants fed upon by pea aphids release volatiles that attract parasitic wasps, and the pea aphid can carry facultative endosymbiotic bacteria that prevent the development of the parasitic wasp larva and thus markedly improve aphid survival after wasp attack. We show that these endosymbionts also attenuate the systemic release of volatiles by plants after aphid attack, reducing parasitic wasp recruitment and increasing aphid fitness. Our results reveal a novel mechanism through which symbionts can benefit their hosts and emphasise the importance of considering the microbiome in understanding insect ecological interactions.

Contrasting effects of heat pulses on different trophic levels, an experiment with a herbivore-parasitoid model system.

Under predicted global climate change, species will be gradually exposed to warmer temperatures, and to a more variable climate including more intense and more frequent heatwaves. Increased climatic variability is expected to have different effects on species and ecosystems than gradual warming. A key challenge to predict the impact of climate change is to understand how temperature changes will affect species interactions. Herbivorous insects and their natural enemies belong to some of the largest groups of terrestrial animals, and thus they have a great impact on the functioning of ecosystems and on the services these ecosystems provide. Here we studied the life history traits of the plant-feeding insect Plutella xylostella and its specialist endoparasitoid Diadegma semiclausum, when exposed to a daily heat pulse of 5 or 10°C temperature increase during their entire immature phase. Growth and developmental responses differed with the amplitude of the heat pulse and they were different between host and parasitoid, indicating different thermal sensitivity of the two trophic levels. With a +5°C heat pulse, the adult parasitoids were larger which may result in a higher fitness, whereas a +10°C heat pulse retarded parasitoid development. These results show that the parasitoid is more sensitive than its host to brief intervals of temperature change, and this results in either positive or negative effects on life history traits, depending on the amplitude of the heat pulse. These findings suggest that more extreme fluctuations may disrupt host-parasitoid synchrony, whereas moderate fluctuations may improve parasitoid fitness.

Natural variation in life history strategy of Arabidopsis thaliana determines stress responses to drought and insects of different feeding guilds.

Plants are sessile organisms and, consequently, are exposed to a plethora of stresses in their local habitat. As a result, different populations of a species are subject to different selection pressures leading to adaptation to local conditions and intraspecific divergence. The annual brassicaceous plant Arabidopsis thaliana is an attractive model for ecologists and evolutionary biologists due to the availability of a large collection of resequenced natural accessions. Accessions of A. thaliana display one of two different life cycle strategies: summer and winter annuals. We exposed a collection of 308 European Arabidopsis accessions, that have been genotyped for 250K SNPs, to a range of stresses: one abiotic stress (drought), four biotic stresses (Pieris rapae caterpillars, Plutella xylostella caterpillars, Frankliniella occidentalis thrips and Myzus persicae aphids) and two combined stresses (drought plus P. rapae and Botrytis cinerea fungus plus P. rapae). We identified heritable genetic variation for responses to the different stresses, estimated by narrow-sense heritability. We found that accessions displaying different life cycle strategies differ in their response to stresses. Winter annuals are more resistant to drought, aphids and thrips and summer annuals are more resistant to P. rapae and P. xylostella caterpillars. Summer annuals are also more resistant to the combined stresses of drought plus P. rapae and infection by the fungus Botryris cinerea plus herbivory by P. rapae. Adaptation to drought displayed a longitudinal gradient. Finally, trade-offs were recorded between the response to drought and responses to herbivory by caterpillars of the specialist herbivore P. rapae.

Nonhost diversity and density reduce the strength of parasitoid-host interactions.

The presence of nonprey or nonhosts is known to reduce the strength of consumer- resource interactions by increasing the consumer's effort needed to find its resource. These interference effects can have a stabilizing effect on consumer-resource dynamics, but have also been invoked to explain parasitoid extinctions. To understand how nonhosts affect parasitoids, we manipulated the density and diversity of nonhost aphids using experimental host-parasitoid communities and tested how this affects parasitation efficiency of two aphid parasitoid species. To further study the behavioral response of parasitoids to nonhosts, we tested for changes in parasitoid time allocation in relation to their host-finding strategies. The proportion of successful attacks (attack rate) in both parasitoid species was reduced by the presence of nonhosts. The parasitoid Aphidius megourae was strongly affected by increasing nonhost diversity with the attack rate dropping from 0.39 without nonhosts to 0.05 with high diversity of nonhosts, while Lysiphlebus fabarum responded less strongly, but in a more pronounced way to an increase in nonhost density. Our experiments further showed that increasing nonhost diversity caused host searching and attacking activity levels to fall in A. megourae, but not in L. fabarum, and that A. megourae changed its behavior after a period of time in the presence of nonhosts by increasing its time spent resting. This study shows that nonhost density and diversity in the environment are crucial determinants for the strength of consumer-resource interactions. Their impact upon a consumer's efficiency strongly depends on its host/prey finding strategy as demonstrated by the different responses for the two parasitoid species. We discuss that these trait-mediated indirect interactions between host and nonhost species are important for community stability, acting either stabilizing or destabilizing depending on the level of nonhost density or diversity present.

Interactions between parasitoids and higher order natural enemies: intraguild predation and hyperparasitoids.

Parasitoids kill and live at the expense of their hosts, but they also serve as food for intraguild predators and hyperparasitoids. Natural enemy diversity can thus challenge herbivore suppression by parasitoids, but this depends on the ecological niches of the species involved and their functional diversity. The spatial context is another important layer of complexity, particularly in areas with reduced habitat complexity and increased fragmentation. Parasitoids have evolved strategies to locate their host, but this can be affected by risk of intraguild predation or hyperparasitism. To better understand these interactions we need more long-term experiments and trophic-web studies. This will provide fundamental knowledge, improve pest control, and allow ecologists to better predict the impact of human activities on species extinctions.

Defensive insect symbiont leads to cascading extinctions and community collapse.

Animals often engage in mutualistic associations with microorganisms that protect them from predation, parasitism or pathogen infection. Studies of these interactions in insects have mostly focussed on the direct effects of symbiont infection on natural enemies without studying community-wide effects. Here, we explore the effect of a defensive symbiont on population dynamics and species extinctions in an experimental community composed of three aphid species and their associated specialist parasitoids. We found that introducing a bacterial symbiont with a protective (but not a non-protective) phenotype into one aphid species led to it being able to escape from its natural enemy and increase in density. This changed the relative density of the three aphid species which resulted in the extinction of the two other parasitoid species. Our results show that defensive symbionts can cause extinction cascades in experimental communities and so may play a significant role in the stability of consumer-herbivore communities in the field.

Host size and spatiotemporal patterns mediate the coexistence of specialist parasitoids.

Many insect parasitoids are highly specialized and thus develop on only one or a few related host species, yet some hosts are attacked by many different parasitoid species in nature. For this reason, they have been often used to examine the consequences of competitive interactions. Hosts represent limited resources for larval parasitoid development and thus one competitor usually excludes all others. Although parasitoid competition has been debated and studied over the past several decades, understanding the factors that allow for coexistence among species sharing the same host in the field remains elusive. Parasitoids may be able to coexist on the same host species if they partition host resources according to size, age, or stage, or if their dynamics vary at spatial and temporal scales. One area that has thus far received little experimental attention is if competition can alter host usage strategies in parasitoids that in the absence of competitors attack hosts of the same size in the field. Here, we test this hypothesis with two parasitoid species in the genus Aphytis, both of which are specialized on the citrus pest California red scale Aonidiella aurantii. These parasitoids prefer large scales as hosts and yet coexist in sympatry in eastern parts of Spain. Parasitoids and hosts were sampled in 12 replicated orange groves. When host exploitation by the stronger competitor, A. melinus, was high the poorer competitor, A. chrysomphali, changed its foraging strategy to prefer alternative plant substrates where it parasitized hosts of smaller size. Consequently, the inferior parasitoid species shifted both its habitat and host size as a result of competition. Our results suggest that density-dependent size-mediated asymmetric competition is the likely mechanism allowing for the coexistence of these two species, and that the use of suboptimal (small) hosts can be advantageous under conditions imposed by competition where survival in higher quality larger hosts may be greatly reduced.

Role of Large Cabbage White butterfly male-derived compounds in elicitation of direct and indirect egg-killing defenses in the black mustard.

To successfully exert defenses against herbivores and pathogens plants need to recognize reliable cues produced by their attackers. Up to now, few elicitors associated with herbivorous insects have been identified. We have previously shown that accessory reproductive gland secretions associated with eggs of Cabbage White butterflies (Pieris spp.) induce chemical changes in Brussels sprouts plants recruiting egg-killing parasitoids. Only secretions of mated female butterflies contain minute amounts of male-derived anti-aphrodisiac compounds that elicit this indirect plant defense. Here, we used the black mustard (Brassica nigra) to investigate how eggs of the Large Cabbage White butterfly (Pieris brassicae) induce, either an egg-killing direct [i.e., hypersensitive response (HR)-like necrosis] or indirect defense (i.e., oviposition-induced plant volatiles attracting Trichogramma egg parasitoids). Plants induced by P. brassicae egg-associated secretions expressed both traits and previous mating enhanced elicitation. Treatment with the anti-aphrodisiac compound of P. brassicae, benzyl cyanide (BC), induced stronger HR when compared to controls. Expression of the salicylic (SA) pathway- and HR-marker PATHOGENESIS-RELATED GENE1 was induced only in plants showing an HR-like necrosis. Trichogramma wasps were attracted to volatiles induced by secretion of mated P. brassicae females but application of BC did not elicit the parasitoid-attracting volatiles. We conclude that egg-associated secretions of Pieris butterflies contain specific elicitors of the different plant defense traits against eggs in Brassica plants. While in Brussels sprouts plants anti-aphrodisiac compounds in Pieris egg-associated secretions were clearly shown to elicit indirect defense, the wild relative B. nigra, recognizes different herbivore cues that mediate the defensive responses. These results add another level of specificity to the mechanisms by which plants recognize their attackers.

Early herbivore alert matters: plant-mediated effects of egg deposition on higher trophic levels benefit plant fitness.

Induction of plant defences, specifically in response to herbivore attack, can save costs that would otherwise be needed to maintain defences even in the absence of herbivores. However, plants may suffer considerable damage during the time required to mount these defences against an attacker. This could be resolved if plants could respond to early cues, such as egg deposition, that reliably indicate future herbivory. We tested this hypothesis in a field experiment and found that egg deposition by the butterfly Pieris brassicae on black mustard (Brassica nigra) induced a plant response that negatively affected feeding caterpillars. The effect cascaded up to the third and fourth trophic levels (larval parasitoids and hyperparasitoids) by affecting the parasitisation rate and parasitoid performance. Overall, the defences induced by egg deposition had a positive effect on plant seed production and may therefore play an important role in the evolution of plant resistance to herbivores.

Phytohormone mediation of interactions between herbivores and plant pathogens.

Induced plant defenses against either pathogens or herbivore attackers are regulated by phytohormones. These phytohormones are increasingly recognized as important mediators of interactions between organisms associated with plants. In this review, we discuss the role of plant defense hormones in sequential tri-partite interactions among plants, pathogenic microbes, and herbivorous insects, based on the most recent literature. We discuss the importance of pathogen trophic strategy in the interaction with herbivores that exhibit different feeding modes. Plant resistance mechanisms also affect plant quality in future interactions with attackers. We discuss exemplary evidence for the hypotheses that (i) biotrophic pathogens can facilitate chewing herbivores, unless plants exhibit effector-triggered immunity, but (ii) facilitate or inhibit phloem feeders. (iii) Necrotrophic pathogens, on the other hand, can inhibit both phloem feeders and chewers. We also propose herbivore feeding mode as predictor of effects on pathogens of different trophic strategies, providing evidence for the hypotheses that (iv) phloem feeders inhibit pathogen attack by increasing SA induction, whereas (v) chewing herbivores tend not to affect necrotrophic pathogens, while they may either inhibit or facilitate biotrophic pathogens. Putting these hypotheses to the test will increase our understanding of phytohormonal regulation of plant defense to sequential attack by plant pathogens and insect herbivores. This will provide valuable insight into plant-mediated ecological interactions among members of the plant-associated community.

Life-history consequences of chronic nutritional stress in an outbreaking insect defoliator.

Food shortage is a common situation in nature but little is known about the strategies animals use to overcome it. This lack of knowledge is especially true for outbreaking insects, which commonly experience nutritional stress for several successive generations when they reach high population densities. The aim of this study is to evaluate the life history consequences of chronic nutritional stress in the outbreaking moth Choristoneura fumiferana. Larvae were reared on two different artificial diets that emulate nutritional conditions larvae face during their natural population density cycle (low and medium quality artificial diets). After four generations, a subset of larvae was fed on the same diet as their parents, and another on the opposite diet. We explored larval life-history strategies to cope with nutritional stress, its associated costs and the influence of nutritional conditions experienced in the parental generation. We found no evidence of nutritional stress in the parental generation increasing offspring ability to feed on low quality diet, but the contrary: compared to offspring from parents that were fed a medium quality diet, larvae from parents fed a low quality diet had increased mortality, reduced growth rate and reduced female reproductive output. Our results support a simple stress hypothesis because the negative effects of malnutrition accumulated over successive generations. Density-dependent deterioration in plant quality is thought to be an important factor governing the population dynamics of outbreaking insects and we hypothesize that chronic nutritional stress can be a driver of outbreak declines of C. fumiferana, and of forest insects in general.