Evolution of conflict and cooperation of nematodes associated with solitary and social sweat bees

Parasites and mutualists can wield great influence on the fitness of social organisms, yet the effect that the host’s social structure has on the evolution of parasites, commensals, and mutualists (collectively referred to here as symbionts) is poorly known. Evolutionary theory suggests that host social structure may select for more cooperative symbiont strains in comparison to symbionts of solitary hosts. We compared the productivity of one social and one solitary bee species (Halictus ligatus and Augochlora pura) in the family Halictidae with and without the presence of their nematode symbionts (Acrostichus halicti and Acrostichus puri, respectively). We measured the number of offspring produced, the number of cells provisioned, and nesting activity (for Au. pura) to test the hypothesis that symbionts specific to a social host exhibit greater cooperation than symbionts specific to a solitary host. Infected and uninfected nests of both species did not differ in any fitness estimates indicating that: (1) Acrostichus species are commensals, or at least lack large fitness effects on their hosts, and (2) the transition from association with a solitary host to association with a social host that lives in small colonies does not have detectable effects on the evolution of conflict and cooperation in this system. This is the first comparative study to test the idea that host social structure may influence the evolution of symbionts; future work should compare closely related mutualists and parasites of more advanced eusocial insects to mutualists and parasites of solitary insects.     

Molecular interactions between bacterial symbionts and their hosts

Symbiotic bacteria are important in animal hosts, but have been largely overlooked as they have proved difficult to culture in the laboratory. Approaches such as comparative genomics and real-time PCR have provided insights into the molecular mechanisms that underpin symbiont-host interactions. Studies on the heritable symbionts of insects have yielded valuable information about how bacteria infect host cells, avoid immune responses, and manipulate host physiology. Furthermore, some symbionts use many of the same mechanisms as pathogens to infect hosts and evade immune responses. Here we discuss what is currently known about the interactions between bacterial symbionts and their hosts.     

Loss and resiliency of social amoeba symbiosis under simulated warming

Anthropogenic global change is increasingly raising concerns about collapses of symbiotic interactions worldwide. Therefore, understanding how climate change affects symbioses remains a challenge and demands more study. Here, we look at how simulated warming affects the social ameba Dictyostelium discoideum and its relationship with its facultative bacterial symbionts, Paraburkholderia hayleyella and Paraburkholderia agricolaris. We cured and cross‐infected ameba hosts with different symbionts. We found that warming significantly decreased D. discoideum''s fitness, and we found no sign of local adaptation in two wild populations. Experimental warming had complex effects on these symbioses with responses determined by both symbiont and host. Neither of these facultative symbionts increases its hosts’ thermal tolerance. The nearly obligate symbiont with a reduced genome, P. hayleyella, actually decreases D. discoideum''s thermal tolerance and even causes symbiosis breakdown. Our study shows how facultative symbioses may have complex responses to global change.     

Can interspecies affairs in the dark lead to evolutionary innovation?

Evolutionary adaptation is the adjustment of species to a new or changing environment. Engaging in mutualistic microbial symbioses has been put forward as a key trait that promotes the differential, evolutionary success of many animal and plant lineages (McFall‐Ngai, 2008). Microbial mutualists allow these organisms to occupy new ecological niches where they could not have persisted on their own or would have been constrained by competitors. Vertical transmission of beneficial microbial symbionts from parents to the offspring is expected to link the adaptive association between a given host and microbe, and it can lead to coevolution and sometimes even cospeciation (Fisher, Henry, Cornwallis, Kiers, & West, 2017). Vertical transmission also causes bottlenecks that strongly reduce the effective population size and genetic diversity of the symbiont population. Moreover, vertically transmitted symbionts are assumed to have fewer opportunities to exchange genes with relatives in the environment. In a “From the Cover” article in this issue of Molecular Ecology, Breusing, Johnson, Vrijenhoek, and Young (2019) investigated whether hybridization among different host species could lead to interspecies exchange of otherwise strictly vertically transmitted symbionts. Hybridization of divergent lineages can potentially cause intrinsic and extrinsic incompatibilities, swamp rare alleles, and lead to population extinctions. In some cases, however, it might also create novel trait combinations that lead to evolutionary innovation (Marques, Meier, & Seehausen, 2019). Breusing et al. (2019) linked the concept of hybridization to symbiont transmission, and their findings have significant implications for the study of evolution of vertically transmitted symbionts and their hosts.     

Genome evolution in bacterial endosymbionts of insects

Many insect species rely on intracellular bacterial symbionts for their viability and fecundity. Large-scale DNA-sequence analyses are revealing the forces that shape the evolution of these bacterial associates and the genetic basis of their specialization to an intracellular lifestyle. The full genome sequences of two obligate mutualists, Buchnera aphidicola of aphids and Wigglesworthia glossinidia of tsetse flies, reveal substantial gene loss and an integration of host and symbiont metabolic functions. Further genomic comparisons should reveal the generality of these features among bacterial mutualists and the extent to which they are shared with other intracellular bacteria, including obligate pathogens.     

Social insect symbionts: evolution in homeostatic fortresses

The massive environmentally buffered nests of some social insects can contain millions of individuals and a wide variety of parasites, commensals and mutualists. We suggest that the ways in which these homeostatic fortress environments affect the evolution of social insect symbionts are relevant for epidemiology, evolutionary biology and macroecology. We contend that specialized parasites will tend to become less virulent and mutualists less cooperative, compared to those associated with solitary or small-colony hosts. These processes are expected to contribute to the very high symbiont diversity observed in these nests. We hypothesize that biodiversity gradients in these hotspots might be less affected by abiotic latitudinal clines than gradients in neighboring 'control' habitats. We suggest several research lines to test these ideas.     

Complex life cycles and the responses of insects to climate change

Many organisms have complex life cycles with distinct life stages that experience different environmental conditions. How does the complexity of life cycles affect the ecological and evolutionary responses of organisms to climate change? We address this question by exploring several recent case studies and synthetic analyses of insects. First, different life stages may inhabit different microhabitats, and may differ in their thermal sensitivities and other traits that are important for responses to climate. For example, the life stages of Manduca experience different patterns of thermal and hydric variability, and differ in tolerance to high temperatures. Second, life stages may differ in their mechanisms for adaptation to local climatic conditions. For example, in Colias, larvae in different geographic populations and species adapt to local climate via differences in optimal and maximal temperatures for feeding and growth, whereas adults adapt via differences in melanin of the wings and in other morphological traits. Third, we extend a recent analysis of the temperature-dependence of insect population growth to demonstrate how changes in temperature can differently impact juvenile survival and adult reproduction. In both temperate and tropical regions, high rates of adult reproduction in a given environment may not be realized if occasional, high temperatures prevent survival to maturity. This suggests that considering the differing responses of multiple life stages is essential to understand the ecological and evolutionary consequences of climate change.     

Studying stress responses in the post-genomic era: its ecological and evolutionary role

Most investigations on the effects of and responses to stress exposures have been performed on a limited number of model organisms in the laboratory. Here much progress has been made in terms of identifying and describing beneficial and detrimental effects of stress, responses to stress and the mechanisms behind stress tolerance. However, to gain further understanding of which genes are involved in stress resistance and how the responses are regulated from an ecological and evolutionary perspective there is a need to combine studies on multiple levels of biological organization from DNA to phenotypes. Furthermore, we emphasize the importance of studying ecologically relevant traits and natural or semi-natural conditions to verify whether the results obtained are representative of the ecological and evolutionary processes in the field. Here, we will review what we currently know about thermal adaptation and the role of different stress responses to thermal challenges in insects, particularly Drosophila. Furthermore, we address some key questions that require future attention.     

昆虫共生菌的垂直传播

共生菌普遍存在于昆虫体内,它们能够为宿主昆虫提供生长发育所必需的氨基酸、固醇类等营养物质,还能提高昆虫适应高温、寄生虫、病毒等不利环境因素的能力,昆虫则为共生菌提供稳定的生存环境和营养物质,昆虫与共生菌相互依存。多数情况下,共生菌通过垂直传播在宿主代次间进行传播,即共生菌由母代传递给子代。结合最近几年相关研究,本文综述了不同昆虫共生菌的垂直传播模式。除极少数肠道共生菌通过污染卵壳被宿主幼虫取食得以垂直传播外,垂直传播的共生菌多为经卵传播。根据侵染时期的不同,共生菌经卵传播模式多数可分为以下4种：侵染宿主昆虫幼虫中的生殖干细胞、侵染宿主昆虫年轻雌成虫中的生殖干细胞、侵染宿主昆虫雌成虫中的成熟卵母细胞以及侵染宿主昆虫囊胚期胚胎。其中,有些共生菌是以共生菌菌胞整体侵染的方式进入到宿主卵巢。另外,少数肠道共生菌也通过卵巢进行垂直传播,此类共生菌先侵染卵巢侧输卵管并在侧输卵管聚集,待卵排放至侧输卵管时再进入到卵中。在文中,我们也探讨了昆虫共生菌垂直传播过程中的细胞机制和免疫机制,包括共生菌避开宿主免疫反应、共生菌通过内吞作用进入卵巢以及不同共生菌间的协同作用等。     

Sex-specific behavioural symptoms of viral gut infection and Wolbachia in Drosophila melanogaster

All organisms are infected with a range of symbionts spanning the spectrum of beneficial mutualists to detrimental parasites. The fruit fly Drosophila melanogaster is a good example, as both endosymbiotic Wolbachia, and pathogenic Drosophila C Virus (DCV) commonly infect it. While the pathophysiology and immune responses against both symbionts are the focus of intense study, the behavioural effects of these infections have received less attention. Here we report sex-specific behavioural responses to these infections in D. melanogaster. DCV infection caused increased sleep in female flies, but had no detectable effect in male flies. The presence of Wolbachia did not reduce this behavioural response to viral infection. We also found evidence for a sex-specific cost of Wolbachia, as male flies infected with the endosymbiont became more lethargic when awake. We discuss these behavioural symptoms as potentially adaptive sickness behaviours.     

Bacterial symbionts in insects or the story of communities affecting communities

Bacterial symbionts are widespread in insects and other animals. Most of them are predominantly vertically transmitted, along with their hosts' genes, and thus extend the heritable genetic variation present in one species. These passengers have a variety of repercussions on the host's phenotypes: besides the cost imposed on the host for maintaining the symbiont population, they can provide fitness advantages to the host or manipulate the host's reproduction. We argue that insect symbioses are ideal model systems for community genetics. First, bacterial symbionts directly or indirectly affect the interactions with other species within a community. Examples include their involvement in modifying the use of host plants by phytophagous insects, in providing resistance to natural enemies, but also in reducing the global genetic diversity or gene flow between populations within some species. Second, one emerging picture in insect symbioses is that many species are simultaneously infected with more than one symbiont, which permits studying the factors that shape bacterial communities; for example, horizontal transmission, interactions between host genotype, symbiont genotype and the environment and interactions among symbionts. One conclusion is that insects' symbiotic complements are dynamic communities that affect and are affected by the communities in which they are embedded.     

A Cross-Taxon Analysis of Insect-Associated Bacterial Diversity

Although it is well known that plants and animals harbor microbial symbionts that can influence host traits, the factors regulating the structure of these microbial communities often remain largely undetermined. This is particularly true for insect-associated microbial communities, as few cross-taxon comparisons have been conducted to date. To address this knowledge gap and determine how host phylogeny and ecology affect insect-associated microbial communities, we collected 137 insect specimens representing 39 species, 28 families, and 8 orders, and characterized the bacterial communities associated with each specimen via 16S rRNA gene sequencing. Bacterial taxa within the phylum Proteobacteria were dominant in nearly all insects sampled. On average, the insect-associated bacterial communities were not very diverse, with individuals typically harboring fewer than 8 bacterial phylotypes. Bacterial communities also tended to be dominated by a single phylotype; on average, the most abundant phylotype represented 54.7% of community membership. Bacterial communities were significantly more similar among closely related insects than among less-related insects, a pattern driven by within-species community similarity but detected at every level of insect taxonomy tested. Diet was a poor predictor of bacterial community composition. Individual insect species harbored remarkably unique communities: the distribution of 69.0% of bacterial phylotypes was limited to unique insect species, whereas only 5.7% of phylotypes were detected in more than five insect species. Together these results suggest that host characteristics strongly regulate the colonization and assembly of bacterial communities across insect lineages, patterns that are driven either by co-evolution between insects and their symbionts or by closely related insects sharing conserved traits that directly select for similar bacterial communities.     

Aphid specialism as an example of ecological–evolutionary divergence

Debate still continues around the definition of generalism and specialism in nature. To some, generalism is equated solely with polyphagy, but this cannot be readily divorced from other essential biological factors, such as morphology, behaviour, genetics, biochemistry, chemistry and ecology, including chemical ecology. Viewed in this light, and accepting that when living organisms evolve to fill new ecological–evolutionary niches, this is the primal act of specialisation, then perhaps all living organisms are specialist in the broadest sense. To illustrate the levels of specialisation that may be found in a group of animals, we here provide an overview of those displayed by a subfamily of hemipteran insects, the Aphididae, which comprises some 1600 species/subspecies in Europe alone and whose members are specialised in a variety of lifestyle traits. These include life cycle, host adaptation, dispersal and migration, associations with bacterial symbionts (in turn related to host adaptation and resistance to hymenopterous wasp parasitoids), mutualisms with ants, and resistance to insecticides. As with polyphagy, these traits cannot easily be separated from one another, but rather, are interconnected, often highly so, which makes the Aphididae a fascinating animal group to study, providing an informative, perhaps unique, model to illustrate the complexities of defining generalism versus specialism.     

Congruent genetic structure in the lichen-forming fungus Lobaria pulmonaria and its green-algal photobiont

The extent of codispersal of symbionts is one of the key factors shaping genetic structures of symbiotic organisms. Concordant patterns of genetic structure are expected in vertically transmitted symbioses, whereas horizontal transmission generally uncouples genetic structures unless the partners are coadapted. Here, we compared the genetic structures of mutualists, the lichen-forming fungus Lobaria pulmonaria and its primary green-algal photobiont, Dictyochloropsis reticulata. We performed analysis of molecular variance and variogram analysis to compare genetic structures between symbiosis partners. We simulated the expected number of multilocus-genotype recurrences to reveal whether the distribution of multilocus genotypes of either species was concordant with panmixia. Simulations and tests of linkage disequilibrium provided compelling evidence for the codispersal of mutualists. To test whether genotype associations between symbionts were consistent with randomness, as expected under horizontal transmission, we simulated the recurrence of fungal-algal multilocus genotype associations expected by chance. Our data showed nonrandom associations of fungal and algal genotypes. Either vertical transmission or horizontal transmission coupled with coadaptation between symbiont genotypes may have created these nonrandom associations. This study is among the first to show codispersal and highly congruent genetic structures in the partners of a lichen mutualism.     

Evolutionary diversification of the gall midge genus Asteromyia (Cecidomyiidae) in a multitrophic ecological context

Gall-forming insects provide ideal systems to analyze the evolution of host–parasite interactions and understand the ecological interactions that contribute to evolutionary diversification. Flies in the family Cecidomyiidae represent the largest radiation of gall-forming insects and are characterized by complex trophic interactions with plants, fungal symbionts, and predators. We analyzed the phylogenetic history and evolutionary associations of the North American cecidomyiid genus Asteromyia, which is engaged in a complex and perhaps co-evolving community of interactions with host-plants, fungi, and parasitoids. Mitochondrial gene trees generally support current classifications, but reveal extensive cryptic diversity within the eight named species. Asteromyia likely radiated after their associated host-plants in the Astereae, but species groups exhibit strong associations with specific lineages of Astereae. Evolutionary associations with fungal mutualists are dynamic, however, and suggest rapid and perhaps coordinated changes across trophic levels.     

Flexibility of nutritional strategies within a mutualism: food availability affects algal symbiont productivity in two congeneric sea anemone species

Mutualistic symbioses are common, especially in nutrient-poor environments where an association between hosts and symbionts can allow the symbiotic partners to persist and collectively out-compete non-symbiotic species. Usually these mutualisms are built on an intimate transfer of energy and nutrients (e.g. carbon and nitrogen) between host and symbiont. However, resource availability is not consistent, and the benefit of the symbiotic association can depend on the availability of resources to mutualists. We manipulated the diets of two temperate sea anemone species in the genus Anthopleura in the field and recorded the responses of sea anemones and algal symbionts in the family Symbiodiniaceae to our treatments. Algal symbiont density, symbiont volume and photosynthetic efficiency of symbionts responded to changes in sea anemone diet, but the responses depended on the species of sea anemone. We suggest that temperate sea anemones and their symbionts can respond to changes in anemone diet, modifying the balance between heterotrophy and autotrophy in the symbiosis. Our data support the hypothesis that symbionts are upregulated or downregulated based on food availability, allowing for a flexible nutritional strategy based on external resources.     

Bacterial symbiosis and paratransgenic control of vector-borne Chagas disease

The triatomine vectors of Chagas disease are obligate haematophagous insects, feeding on vertebrate blood throughout their entire developmental cycle. As a result of obtaining their nutrition from a single food source, their diet is devoid of certain vitamins and nutrients. Consequently, these insects harbour populations of bacterial symbionts within their intestinal tract, which provide the required nutrients that are lacking from their diet. We have isolated and characterised symbiont cultures from various triatomine species and developed a method for genetically transforming them. We can then reintroduce them into their original host species, thereby producing stable paratransgenic insects in which we are able to express heterologous gene products. Using this methodology, we have generated paratransgenic Rhodnius prolixus that are refractory for infection with Trypanosoma cruzi. Two examples of potentially refractory genes are currently being expressed in paratransgenic insects. These include the insect immune peptide cecropin A and active single chain antibody fragments. We have also developed an approach that would allow introduction of genetically modified bacterial symbionts into natural populations of Chagas disease vectors. This approach utilises the coprophagic behaviour of these insects, which is the way in which the symbionts are transmitted among bug populations in nature. The production and ultimate release of transgenic or paratransgenic insects for public health applications is potentially very promising but also worthy of much careful consideration with respect to environmental, political, and human safety concerns.     

Are we underestimating the diversity and incidence of insect bacterial symbionts? A case study in ladybird beetles

Vertically transmitted bacterial symbionts are common in arthropods. However, estimates of their incidence and diversity are based on studies that test for a single bacterial genus and often only include small samples of each host species. Focussing on ladybird beetles, we collected large samples from 21 species and tested them for four different bacterial symbionts. Over half the species were infected, and there were often multiple symbionts in the same population. In most cases, more females than males were infected, suggesting that the symbionts may be sex ratio distorters. Many of these infections would have been missed in previous studies as they only infect a small proportion of the population. Furthermore, 11 out of the 17 symbionts discovered by us were either in the genus Rickettsia or Spiroplasma, which are rarely sampled. Our results suggest that the true incidence and diversity of bacterial symbionts in insects may be far greater than previously thought.