PHYTOPHAGOUS INSECT–MICROBE MUTUALISMS AND ADAPTIVE EVOLUTIONARY DIVERSIFICATION

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect–microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

An omics evolutionary perspective on phytophagous insect–host plant interactions in Anastrepha obliqua: a review

Phytophagous insects have a close relationship with their host plants. For this reason, their interactions can lead to important changes in insect population dynamics and evolutionary trajectories. Next generation sequencing (NGS) has provided an opportunity to analyze omics data on a large scale, facilitating the change from a classical genetics approach to a more holistic understanding of the underlying molecular mechanisms of host plant use by insects. Most studies have been carried out on model species in Holarctic and temperate zones. In tropical zones, however, the effects of use of various host plants on evolutionary insect history is less understood. In the current review, we describe how omics methodologies help us to understand phytophagous insect–host plant interactions from an evolutionary perspective, using as example the Neotropical phytophagous insect West Indian fruit fly, Anastrepha obliqua (Macquart) (Diptera: Tephritidae), an economically important fruit crop pest in the Americas. Anastrepha obliqua could adopt a generalist or a specialist lifestyle. We first review the adaptive molecular mechanisms of phytophagous insects to host plants, and then describe the main tools to study phytophagous insect–host plant interactions in the era of omics sciences. The omics approaches will advance the understanding of insect molecular mechanisms and their influence on diversification and evolution. Finally, we discuss the importance of a multidisciplinary approach that integrates the use of omics tools and other, more classical methodologies in evolutionary studies.     

The tri‐trophic niche concept and adaptive radiation of phytophagous insects

A conceptual divide exists between ecological and evolutionary approaches to understanding adaptive radiation, although the phenomenon is inherently both ecological and evolutionary. This divide is evident in studies of phytophagous insects, a highly diverse group that has been frequently investigated with the implicit or explicit goal of understanding its diversity. Whereas ecological studies of phytophagous insects increasingly recognize the importance of tri‐trophic interactions as determinants of niche dimensions such as host‐plant associations, evolutionary studies typically neglect the third trophic level. Here we attempt to reconcile ecological and evolutionary approaches through the concept of the ecological niche. We specifically present a tri‐trophic niche concept as a foil to the traditional bi‐trophic niche concept for phytophagous insects. We argue that these niche concepts have different implications for understanding herbivore community structure, population divergence, and evolutionary diversification. To this end, we offer contrasting empirical predictions of bi‐ and tri‐trophic niche concepts for patterns of community structure, the process of population divergence, and patterns of evolutionary diversification of phytophagous insects.     

Cheating and the evolutionary stability of mutualisms

Interspecific mutualisms have been playing a central role in the functioning of all ecosystems since the early history of life. Yet the theory of coevolution of mutualists is virtually nonexistent, by contrast with well-developed coevolutionary theories of competition, predator-prey and host-parasite interactions. This has prevented resolution of a basic puzzle posed by mutualisms: their persistence in spite of apparent evolutionary instability. The selective advantage of 'cheating', that is, reaping mutualistic benefits while providing fewer commodities to the partner species, is commonly believed to erode a mutualistic interaction, leading to its dissolution or reciprocal extinction. However, recent empirical findings indicate that stable associations of mutualists and cheaters have existed over long evolutionary periods. Here, we show that asymmetrical competition within species for the commodities offered by mutualistic partners provides a simple and testable ecological mechanism that can account for the long-term persistence of mutualisms. Cheating, in effect, establishes a background against which better mutualists can display any competitive superiority. This can lead to the coexistence and divergence of mutualist and cheater phenotypes, as well as to the coexistence of ecologically similar, but unrelated mutualists and cheaters.     

Genetic diversity of termite-egg mimicking fungi “termite balls” within the nests of termites

Antagonistic or mutualistic interactions between insects and fungi are well-known, and the mutualistic interactions of fungus-growing ants, fungus-growing termites, and fungus-gardening beetles with their respective fungal mutualists are model examples of coevolution. However, our understanding of coevolutionary interactions between insects and fungi has been based on a few model systems. Fungal mimicry of termite eggs is one of the most striking evolutionary consequences of insect–fungus associations. This novel termite–fungus interaction is a good model system to compare with the relatively well-studied systems of fungus-growing ants and termites because termite egg-mimicking fungi are protected in the nests of social insects, as are fungi cultivated by fungus-growing ants and termites. Recently, among systems of fungus-growing ants and termites, much attention has been focused on common factors including monoculture system for the ultimate evolutionary stability of mutualism. We examined the genetic diversity of termite egg-mimicking fungi within host termite nests. RFLP analysis demonstrated that termite nests were often infected by multiple strains of termite egg-mimicking fungi, in contrast to single-strain monocultures in fungus combs of fungus-growing ants and termites. Additionally, phylogenetic analyses indicated the existence of a free-living stage of the termite egg-mimicking fungus as well as frequent long-distance gene flow by spores and subsequent horizontal transmission. Comparisons of these results with previous studies of fungus-growing ants and termites suggest that the level of genetic diversity of fungal symbionts within social insect nests may be important in shaping the outcome of the coevolutionary interaction, despite the fact that the mechanism for achieving genetic diversity varies with the evolutionary histories of the component species.     

Evolutionary origins and diversification of proteobacterial mutualists

Mutualistic bacteria infect most eukaryotic species in nearly every biome. Nonetheless, two dilemmas remain unresolved about bacterial–eukaryote mutualisms: how do mutualist phenotypes originate in bacterial lineages and to what degree do mutualists traits drive or hinder bacterial diversification? Here, we reconstructed the phylogeny of the hyperdiverse phylum Proteobacteria to investigate the origins and evolutionary diversification of mutualistic bacterial phenotypes. Our ancestral state reconstructions (ASRs) inferred a range of 34–39 independent origins of mutualist phenotypes in Proteobacteria, revealing the surprising frequency with which host-beneficial traits have evolved in this phylum. We found proteobacterial mutualists to be more often derived from parasitic than from free-living ancestors, consistent with the untested paradigm that bacterial mutualists most often evolve from pathogens. Strikingly, we inferred that mutualists exhibit a negative net diversification rate (speciation minus extinction), which suggests that mutualism evolves primarily via transitions from other states rather than diversification within mutualist taxa. Moreover, our ASRs infer that proteobacterial mutualist lineages exhibit a paucity of reversals to parasitism or to free-living status. This evolutionary conservatism of mutualism is contrary to long-standing theory, which predicts that selection should often favour mutants in microbial mutualist populations that exploit or abandon more slowly evolving eukaryotic hosts.     

Insect endosymbionts: manipulators of insect herbivore trophic interactions?

Throughout their evolutionary history, insects have formed multiple relationships with bacteria. Although many of these bacteria are pathogenic, with deleterious effects on the fitness of infected insects, there are also numerous examples of symbiotic bacteria that are harmless or even beneficial to their insect host. Symbiotic bacteria that form obligate or facultative associations with insects and that are located intracellularly in the host insect are known as endosymbionts. Endosymbiosis can be a strong driving force for evolution when the acquisition and maintenance of a microorganism by the insect host results in the formation of novel structures or changes in physiology and metabolism. The complex evolutionary dynamics of vertically transmitted symbiotic bacteria have led to distinctive symbiont genome characteristics that have profound effects on the phenotype of the host insect. Symbiotic bacteria are key players in insect–plant interactions influencing many aspects of insect ecology and playing a key role in shaping the diversification of many insect groups. In this review, we discuss the role of endosymbionts in manipulating insect herbivore trophic interactions focussing on their impact on plant utilisation patterns and parasitoid biology.     

The cryptic role of biodiversity in the emergence of host–microbial mutualisms

The persistence of mutualisms in host‐microbial – or holobiont – systems is difficult to explain because microbial mutualists, who bear the costs of providing benefits to their host, are always prone to being competitively displaced by non‐mutualist ‘cheater’ species. This disruptive effect of competition is expected to be particularly strong when the benefits provided by the mutualists entail costs such as reduced competitive ability. Using a metacommunity model, we show that competition between multiple cheaters within the host's microbiome, when combined with the spatial structure of host–microbial interactions, can have a constructive rather than a disruptive effect by allowing the emergence and maintenance of mutualistic microorganisms within the host. These results indicate that many of the microorganisms inhabiting a host's microbiome, including those that would otherwise be considered opportunistic or even potential pathogens, play a cryptic yet critical role in promoting the health and persistence of the holobiont across spatial scales.     

Insect-plant interactions on a planet of weeds

Two conflicting views confront ecologists and evolutionary biologists on the degree of symmetry in interactions between plants and phytophagous insects. The symmetrical view holds that insects and plants have strong effects on one another's evolutionary and ecological dynamics. Thus, herbivores are regarded as a major influence on plant distribution and abundance in contemporary ecosystems, and coevolution is commonly invoked to explain adaptive radiation in plants and insects, host specialization in insects, as well as much of the morphological and chemical variety observed in plants. The asymmetrical view acknowledges that plants have major effects on insects, but claims that insects seldom impose significant effects on plants. Proponents of the asymmetric view tend to ignore or discount insect-plant interactions in communities and ecosystems altered by human impacts. If we recognize the scope and scale of human impacts, and ways in which these impacts change insect-plant interactions, then our views about symmetry or asymmetry in insect-plant interactions will change. To understand, predict, and manage insect herbivory we need to study it in all its manifestations. In particular, the study of interactions involving alien species is both an urgent priority for environmental management and potentially a source of ecological insights on the role of herbivores in plant population and community dynamics. A complete theory of insect/host plant interactions must explain and predict interactions both within and beyond the native range. Such a theory might guide efforts to deal with environmental problems stemming from rapid rates of extinction and homogenization of the world's biota.     

Butterfly host plant range: an example of plasticity as a promoter of speciation?

Mary Jane West-Eberhard has suggested that plasticity may be of primary importance in promoting evolutionary innovation and diversification. Here, we explore the possibility that the diversification of phytophagous insects may have occurred through such a process, using examples from nymphalid butterflies. We discuss the ways in which host plant range is connected to plasticity and present our interpretation of how West-Eberhard’s scenario may result in speciation driven by plasticity in host utilization. We then review some of the evidence that diversity of plant utilization has driven the diversification of phytophagous insects and finally discuss whether this suggests a role for plasticity-driven speciation. We find a close conceptual connection between our theory that the diversification of phytophagous insects has been driven by oscillations in host range, and our personal interpretation of the most efficient way in which West-Eberhard’s theory could account for plasticity-driven speciation. A major unresolved issue is the extent to which a wide host plant range is due to adaptive plasticity with dedicated modules of genetic machinery for utilizing different plants.     

The evolution of plant-insect mutualisms

Mutualisms (cooperative interactions between species) have had a central role in the generation and maintenance of life on earth. Insects and plants are involved in diverse forms of mutualism. Here we review evolutionary features of three prominent insect-plant mutualisms: pollination, protection and seed dispersal. We focus on addressing five central phenomena: evolutionary origins and maintenance of mutualism; the evolution of mutualistic traits; the evolution of specialization and generalization; coevolutionary processes; and the existence of cheating. Several features uniting very diverse insect-plant mutualisms are identified and their evolutionary implications are discussed: the involvement of one mobile and one sedentary partner; natural selection on plant rewards; the existence of a continuum from specialization to generalization; and the ubiquity of cheating, particularly on the part of insects. Plant-insect mutualisms have apparently both arisen and been lost repeatedly. Many adaptive hypotheses have been proposed to explain these transitions, and it is unlikely that any one of them dominates across interactions differing so widely in natural history. Evolutionary theory has a potentially important, but as yet largely unfilled, role to play in explaining the origins, maintenance, breakdown and evolution of insect-plant mutualisms.     

Phylogenetic and Experimental Tests of Interactions among Mutualistic Plant Defense Traits in Viburnum (Adoxaceae)

Abstract Plant traits that mediate mutualistic interactions are widespread, yet few studies have linked their macroevolutionary patterns with the ecological interactions they mediate. Here we merged phylogenetic and experimental approaches to investigate the evolution of two common mutualistic plant traits, extrafloral nectaries (EFNs) and leaf domatia. By using the flowering plant clade Viburnum, we tested whether macroevolutionary patterns support adaptive hypotheses and conducted field surveys and manipulative experiments to examine whether ecological interactions are concordant with evolutionary predictions. Phylogenetic reconstructions suggested that EFN-bearing species are monophyletic, whereas the evolution of domatia correlated with leaf production strategy (deciduous or evergreen) and climate. Domatia were also more common in the EFN clade, suggesting that the two traits may jointly mediate ecological interactions. This result was further investigated in a common-garden survey, where plants with domatia and EFNs on the leaf blade had more mutualistic mites than plants with other trait combinations, and in manipulative field experiments, where the traits additively increased mutualist abundance. Taken together, our results suggest that mutualistic traits in Viburnum are not ecologically independent, as they work in concert to attract and retain mutualists, and their long-term evolution may be influenced by complex interactions among multiple traits, mutualists, and geography.     

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.     

Les symbioses entre plantes et fourmis arboricoles

In communities of tree-nesting ants in tropical rain forests, energy-rich resources from plants enable ants to achieve high densities and permit the evolution of energy-intensive strategies of prédation. Ants are more abundant, and can maintain populations of phytophagous insects at lower densities than if ant populations were limited simply by insect prey. A large proportion of woody plants in tropical forests are involved in such loose protection mutualisms. Many epiphytes are also involved in loose associations with ants, in which benefits to plants may include nutrition and seed dispersal as well as protection. From such opportunistic interactions numerous symbiotic mutualisms have evolved, in which ants and plants are more intimately and often more specifically associated. The diversity of these symbiotic interactions between ants and plants make these associations good models for examining many general questions in ecology. Plants that have evolved specialised structures (‘ant-domatia’) to house ants are termed ‘myrmécophytes’ or ‘ant-plants’, and their specialised associates are termed ‘plant-ants’. In these symbioses, plants and ants have coevolved. Ant colonies that provide increased benefits to the host plant enhance its growth and survival, thus receiving more benefits from it, and vice versa. Selection favours mutualistic traits, and interests of the two partners tend to converge. However, because these associations are horizontally transmitted, neither partner obtains benefits from reproduction of the other. Because reproduction draws away resources from growth (from which the partner benefits), it introduces conflicts of interest between ants and plants, and several examples show the importance of such conflicts in the dynamics of coevolution. Antplant coevolution has produced parasites as well as mutualists. Much is still unknown on the evolutionary ecology of these symbioses. Mechanisms of interaction at the chemical level (chemical ecology) are little explored. The functioning of ant-plant associations at the level of populations and communities is poorly understood, and information in this domain is crucial for the conservation of these intricate symbioses in forests increasingly subjected to disturbance and fragmentation.     

Parrots as key multilinkers in ecosystem structure and functioning

Mutually enhancing organisms can become reciprocal determinants of their distribution, abundance, and demography and thus influence ecosystem structure and dynamics. In addition to the prevailing view of parrots (Psittaciformes) as plant antagonists, we assessed whether they can act as plant mutualists in the dry tropical forest of the Bolivian inter‐Andean valleys, an ecosystem particularly poor in vertebrate frugivores other than parrots (nine species). We hypothesised that if interactions between parrots and their food plants evolved as primarily or facultatively mutualistic, selection should have acted to maximize the strength of their interactions by increasing the amount and variety of resources and services involved in particular pairwise and community–wide interaction contexts. Food plants showed different growth habits across a wide phylogenetic spectrum, implying that parrots behave as super‐generalists exploiting resources differing in phenology, type, biomass, and rewards from a high diversity of plants (113 species from 38 families). Through their feeding activities, parrots provided multiple services acting as genetic linkers, seed facilitators for secondary dispersers, and plant protectors, and therefore can be considered key mutualists with a pervasive impact on plant assemblages. The number of complementary and redundant mutualistic functions provided by parrots to each plant species was positively related to the number of different kinds of food extracted from them. These mutually enhancing interactions were reflected in species‐level properties (e.g., biomass or dominance) of both partners, as a likely consequence of the temporal convergence of eco‐(co)evolutionary dynamics shaping the ongoing structure and organization of the ecosystem. A full assessment of the, thus far largely overlooked, parrot–plant mutualisms and other ecological linkages could change the current perception of the role of parrots in the structure, organization, and functioning of ecosystems.     

A general framework for effectiveness concepts in mutualisms

A core interest in studies of mutualistic interactions is the ‘effectiveness’ of mutualists in providing benefits to their partners. In plant‐animal mutualisms it is widely accepted that the total effect of a mutualist on its partner is estimated as (1) a ‘quantity’ component multiplied by (2) a ‘quality’ component, although the meanings of ‘effectiveness,’ ‘quantity,’ and ‘quality’ and which terms are applied to these metrics vary greatly across studies. In addition, a similar quantity × quality = total effect approach has not been applied to other types of mutualisms, although it could be informative. Lastly, when a total effect approach has been applied, it has invariably been from a phytocentric perspective, focussing on the effects of animal mutualists on their plant partner. This lack of a common framework of ‘effectiveness’ of mutualistic interactions limits generalisation and the development of a broader understanding of the ecology and evolution of mutualisms. In this paper, we propose a general framework and demonstrate its utility by applying it to both partners in five different types of mutualisms: pollination, seed dispersal, plant protection, rhizobial, and mycorrhizal mutualisms. We then briefly discuss the flexibility of the framework, potential limitations, and relationship to other approaches.     

Pattern and process in the evolution of insect-plant associations: Yponomeuta as an example

Phylogenetic studies are increasing our understanding of the evolution of associations between phytophagous insects and their host plants. Sequential evolution, i.e. the shift of insect herbivores onto pre-existing plant species, appears to be much more common than coevolution, where reciprocal selection between interacting insects and plants is thought to induce chemical diversification and resistance in plants and food specialization in insects.Extreme host specificity is common in phytophagous insects and future studies are likely to reveal even more specialization. Hypotheses that assume that food specialists have selective advantages over generalists do not seem to provide a general explanation for the ubiquity of specialist insect herbivores. Specialists are probably committed to remain so, because they have little evolutionary opportunity to reverse the process due to genetically determined constraints on the evolution of their physiology or nervous system. The same constraints might result in phylogenetic conservatism, i.e. the frequent association of related insect herbivores with related plants. Current phylogenetic evidence, however, indicates that there is no intrinsic direction to the evolution of specialization.Historical aspects of insect-host plant associations will be illustrated with the small ermine moth genus Yponomeuta. Small ermine moths show an ancestral host association with the family Celastraceae. The genus seems to be committed to specialization per se rather than to a particular group of plants. Whatever host shift they have made in their evolutionary past (onto Rosaceae, Crassulaceae, and Salicaceae), they remain monophagous. The oligophagous Y. padellus is the only exception. This species might comprise a mosaic of genetically divergent host-associated populations.     

Specificity in host-fungus associations: Do mutualists differ from antagonists?

Summary Physically intimate interactions between organisms are assumed to be highly specific, yet intimate mutualisms exhibiting little specificity are common and important in many communities. We compare host records for ectomycorrhizal fungi (mutualists) to those for biotrophic shoot fungi and necrotrophic root fungi (both antagonists) in order to test two alternative predictions: (1) intimate physical associations (biotrophy) are more specific than less intimate ones (necrotrophy); (2) antagonisms are more specific than mutualisms. Specificity of fungi for hosts supports prediction (1): ectomycorrhizal fungi and shoot biotrophs are more host specific than root necrotrophs. Fungal symbiont ranges of hosts supports prediction (2): woody hosts are associated with a greater number of mutualistic fungi than antagonistic fungi. The numbers of fungi in the three groups infecting hosts are all significantly positively correlated. This result suggests that some hosts are resistant to fungal invasion and others are quite susceptible. Thus, plants may not be able to erect selective barriers to only antagonistic fungi. The marked asymmetry of specificity from the perspectives of hosts vs fungi suggests that evolutionary and ecological processes act differently on partners in symbioses.     

论昆虫与植物的相互作用和进化的关系

昆虫与植物是陆地生物群落中最为重要的组成部分,二者间的相互作用是多方面的,其中最为重要的是昆虫选择植物作为食物和生长场所、昆虫为植物传授花粉两方面。该文集中讨论这两方面的相互作用有哪些因素与进化有密切的关系。植食性昆虫根据其寄主植物范围,通常分为专食性（寄主范围窄）和广食性（寄主范围广）。从生态关系来看,广食性的取食行为比专食性的更为有利,但实际情况却与此相反,统观植食性昆虫的取食行为,有向专食性演化更为普遍的倾向。专食性发展有利于提高昆虫对寄主植物的选择效率,还可缓和天敌作用所造成的压力。根据昆虫与植物相互作用的特点,目前已提出很多昆虫与植物的进化理论,包括成对的协同进化、弥散的协同进化、群落的协同进化以及顺序进化。在昆虫对寄主植物的选择中,以植物对昆虫的影响较昆虫对植物的影响更为重要,称为顺序进化是适宜的;昆虫为被子植物传授花粉造成互惠共生,其中的进化关系应称为协同进化。     

Mixed infections may promote diversification of mutualistic symbionts: why are there ineffective rhizobia?

While strategy variation is a key feature of symbiotic mutualisms, little work focuses on the origin of this diversity. Rhizobia strategies range from mutualistic nitrogen fixers to parasitic nonfixers that hoard plant resources to increase their own survival in soil. Host plants reward beneficial rhizobia with higher nodule growth rates, generating a trade‐off between reproduction in nodules and subsequent survival in soil. However, hosts might not discriminate between strains in mixed infections, allowing nonfixing strains to escape sanctions. We construct an adaptive dynamics model of symbiotic nitrogen‐fixation and find general situations where symbionts undergo adaptive diversification, but in most situations complete nonfixers do not evolve. Social conflict in mixed infections when symbionts face a survival–reproduction trade‐off can drive the origin of some coexisting symbiont strategies, where less mutualistic strains exploit benefits generated by better mutualists.