Trait‐based partner selection drives mycorrhizal network assembly

Plants and their microbial symbionts are often found to interact non‐randomly in nature, but we have yet to understand the mechanisms responsible for such preferential species associations. Theory predicts that host plants should select symbiotic partners bearing traits complementary to their own, as this should favor cooperation and evolutionary stability of mutualisms. Here, we present the first field‐based empirical test for this hypothesis using arbuscular mycorrhizas (AM), the oldest and most widespread plant symbiosis. Preferential associations occurring within a local plant–AM fungal community could not be predicted by the spatial distributions of interacting partners, nor by gradients in soil properties. Rather, plants with similar traits preferentially hosted similar AM fungi and, likewise, phylogenetically related AM fungi (assumed to have similar functional traits) interacted with similar plants. Our results suggest that trait‐based partner selection may have been a strong force in maintaining plant–AM fungal symbioses since the evolution of land plants.     

Coevolution by different functional mechanisms modulates the structure and dynamics of antagonistic and mutualistic networks

A central problem in the study of species interactions is to understand the underlying ecological and evolutionary mechanisms that shape and are shaped by trait evolution in interacting assemblages. The patterns of interaction among species (i.e. network structure) provide the pathways for evolution and coevolution, which are modulated by how traits affect individual fitness (i.e. functional mechanisms). Functional mechanisms, in turn, also affect the likelihood of an ecological interaction, shaping the structure of interaction networks. Here, we build adaptive network models to explore the potential role of coevolution by two functional mechanisms, trait matching and exploitation barrier, in driving trait evolution and the structure of interaction networks. We use these models to explore how different scenarios of coevolution and functional mechanisms reproduce the empirical network patterns observed in antagonistic and mutualistic interactions and affect trait evolution. Scenarios assuming coevolutionary feedback with a strong effect of functional mechanism better reproduce the empirical structure of networks. Antagonistic and mutualistic networks, however, are better explained by different functional mechanisms and the structure of antagonisms is better reproduced than that of mutualisms. Scenarios assuming coevolution by strong trait matching between interacting partners better explain the structure of antagonistic networks, whereas those assuming strong barrier effects better reproduce the structure of mutualistic networks. The dynamics resulting from the feedback between strong functional mechanisms and coevolution favor the stability of antagonisms and mutualisms. Selection favoring trait matching reduces temporal trait fluctuation and the magnitude of arms races in antagonisms, whereas selection due to exploitation barriers reduces temporal trait fluctuations in mutualisms. Our results indicate that coevolutionary models better reproduce the network structure of antagonisms than those of mutualisms and that different functional mechanisms may favor the persistence of antagonistic and mutualistic interacting assemblages.     

Dark septate endophytes – are they mycorrhizal?

Dark septate endophytes (DSE) are a miscellaneous group of ascomycetous anamorphic fungi that colonize root tissues intracellularly and intercellularly. The limited selection of studies quoted here exemplifies the range of host responses to symbiotic DSE fungi. Like mycorrhizal associations, DSE associations vary from negative to neutral and positive when measured by host performance or host tissue nutrient concentrations. This range of host responses is partially attributable to variation between different fungus taxa and strains. Similarly, hosts differ in their responses to a single DSE strain. Experimental conditions may also govern the nature of the symbiotic association. It is concluded that DSE are capable of forming mutualistic associations functionally similar to mycorrhizas. If the variation in host response to mycorrhizal fungi is considered to represent a continuum ranging from parasitism to mutualism, DSE symbiosis must be considered mycorrhizal, at least under some conditions.     

Whose trait is it anyways? Coevolution of joint phenotypes and genetic architecture in mutualisms

Evolutionary biologists typically envision a trait’s genetic basis and fitness effects occurring within a single species. However, traits can be determined by and have fitness consequences for interacting species, thus evolving in multiple genomes. This is especially likely in mutualisms, where species exchange fitness benefits and can associate over long periods of time. Partners may experience evolutionary conflict over the value of a multi-genomic trait, but such conflicts may be ameliorated by mutualism’s positive fitness feedbacks. Here, we develop a simulation model of a host–microbe mutualism to explore the evolution of a multi-genomic trait. Coevolutionary outcomes depend on whether hosts and microbes have similar or different optimal trait values, strengths of selection and fitness feedbacks. We show that genome-wide association studies can map joint traits to loci in multiple genomes and describe how fitness conflict and fitness feedback generate different multi-genomic architectures with distinct signals around segregating loci. Partner fitnesses can be positively correlated even when partners are in conflict over the value of a multi-genomic trait, and conflict can generate strong mutualistic dependency. While fitness alignment facilitates rapid adaptation to a new optimum, conflict maintains genetic variation and evolvability, with implications for applied microbiome science.     

Population genetic consequences of feeding habits in some forest lepidoptera

By surveying variation at allozyme loci in several phytophagous lepidopteran species (Geometridae), we have tested two hypotheses about the relationship of genetic variation to environmental heterogeneity: (1) that allozyme polymorphisms may exist because of associations between genotypes and "niches" (different host plants, in this instance), and (2) that the overall genetic variation of a species is correlated with environmental heterogeneity (or breadth of the species' overall ecological niche).—Genetic differentiation among samples of oligophagous or polyphagous species taken from different host species was observed in one of three species, at only one of seven polymorphic loci. The data thus provide no evidence for pronounced genetic substructuring, or "host race" formation in these sexually reproducing species, although host plant-genotype associations in a parthenogenetic moth give evidence of the potential for diversifying selection.—In a comparison of allozyme variation in polyphagous ("generalized") and oligophagous ("specialized") species, heterozygosity appeared to be higher in specialized species, at all polymorphic loci but one. It is possible that this unexpected result arises from a functional relation between breadth of diet and genetic variation.     

Parasites may help stabilize cooperative relationships

Background  

The persistence of cooperative relationships is an evolutionary paradox; selection should favor those individuals that exploit their partners (cheating), resulting in the breakdown of cooperation over evolutionary time. Our current understanding of the evolutionary stability of mutualisms (cooperation between species) is strongly shaped by the view that they are often maintained by partners having mechanisms to avoid or retaliate against exploitation by cheaters. In contrast, we empirically and theoretically examine how additional symbionts, specifically specialized parasites, potentially influence the stability of bipartite mutualistic associations. In our empirical work we focus on the obligate mutualism between fungus-growing ants and the fungi they cultivate for food. This mutualism is exploited by specialized microfungal parasites (genus Escovopsis) that infect the ant's fungal gardens. Using sub-colonies of fungus-growing ants, we investigate the interactions between the fungus garden parasite and cooperative and experimentally-enforced uncooperative ("cheating") pairs of ants and fungi. To further examine if parasites have the potential to help stabilize some mutualisms we conduct Iterative Prisoner's Dilemma (IPD) simulations, a common framework for predicting the outcomes of cooperative/non-cooperative interactions, which incorporate parasitism as an additional factor.     

Plant killing by Neotropical acacia ants: ecology,decision‐making,and head morphology

Mutualistic species often associate with several partners that vary in the benefits provided. In some protective ant–plant mutualisms, ants vary in the extent at which they kill neighboring vegetation. Particularly, in acacia ants (Pseudomyrmex), the area around the host tree that ants keep free from vegetation (“clearings”) vary depending on the species. This study assessed whether interspecific variation in clearing size corresponds to workers biting on plant tissue of different thickness. As expected, workers from species making the largest clearings bit more often on thicker plant tissues than workers from species making smaller clearings. Because head shape affects mandible force, I also assessed whether pruning on thick tissue in mutualistic ant species or being a predator in non‐mutualistic species correlated with broader heads, which yield stronger mandible force. The species with the broader heads were non‐mutualistic predators or mutualistic pruners of thick tissues, which suggest that pruning neighboring vegetation in non‐predatory species demands force even when the ants do not kill prey with their mandibles. The findings reveal that clearing size variation in mutualistic ant partners of plants can also be observed at the level of individual decision‐making processes among workers, and suggest that head morphology could be a trait under selection in protective ant–plant mutualisms. Abstract in Spanish is available with online material.     

Population genetic signatures of diffuse co-evolution between leaf-cutting ants and their cultivar fungi

Switching of symbiotic partners pervades most mutualisms, despite mechanisms that appear to enforce partner fidelity. To investigate the interplay of forces binding and dissolving mutualistic pairings, we investigated partner fidelity at the population level in the attine ant-fungal cultivar mutualism. The ants and their cultivars exhibit both broad-scale co-evolution, as well as cultivar switching, with short-term symbiont fidelity maintained by vertical transmission of maternal garden inoculates via dispersing queens and by the elimination of alien cultivar strains. Using microsatellite markers, we genotyped cultivar fungi associated with five co-occurring Panamanian attine ant species, representing the two most derived genera, leaf-cutters Atta and Acromyrmex. Despite the presence of mechanisms apparently ensuring the cotransmission of symbiont genotypes, different species and genera of ants sometimes shared identical fungus garden genotypes, indicating widespread cultivar exchange. The cultivar population was largely unstructured with respect to host ant species, with only 10% of the structure in genetic variance being attributable to partitioning among ant species and genera. Furthermore, despite significant genetic and ecological dissimilarity between Atta and Acromyrmex, generic difference accounted for little, if any, variance in cultivar population structure, suggesting that cultivar exchange dwarfs selective forces that may act to create co-adaptive ant-cultivar combinations. Thus, binding forces that appear to enforce host fidelity are relatively weak and pairwise associations between cultivar lineages and ant species have little opportunity for evolutionary persistence. This implicates that mechanisms other than partner fidelity feedback play important roles in stabilizing the leafcutter ant-fungus mutualism over evolutionary time.     

The resource-mediated modular structure of a non-symbiotic ant–plant mutualism

1. Plant–animal mutualisms are key processes that influence community structure, dynamics, and function. They reflect several neutral and niche-based mechanisms related to plant–animal interactions. 2. However, the strength with which these processes influence community structure depends on functional traits that influence the interactions between mutualistic partners. In mutualisms involving plants and ants, nectar is the most common reward, and traits such as quantity and quality can affect ant species' responses by influencing their recruitment rates and aggressiveness. 3. In this study, nectar traits that mediate ant–plant defensive mutualisms were manipulated to test whether resource quantity and quality affect the structure of ant–plant interaction networks. A downscaling approach was used to investigate the interaction network between ant species and individual plants of the extrafloral nectary-bearing terrestrial orchid Epidendrum secundum. 4. We found a short-term reorganization of the ant assemblage that caused the interaction networks to become more specialised and modular in response to a more rewarding nectar gradient. Furthermore, the ant species tended to narrow their foraging range by limiting their associations to one or a few individual plants. 5. This study shows that ant species' responses to variable resource traits play an important role in the structure of the ant–plant interaction network. We suggest that more rewarding nectar enhanced aggressiveness and a massive recruitment of some ant species, leading to lower niche overlap and thus a less connected and more specialised network.     

Gene copy-number polymorphism in nature

Differences between individuals in the copy-number of whole genes have been found in every multicellular species examined thus far. Such differences result in unique complements of protein-coding genes in all individuals, and have been shown to underlie adaptive phenotypic differences. Here, we review the evidence for copy-number variants (CNVs), focusing on the methods used to detect them and the molecular mechanisms responsible for generating this type of variation. Although there are multiple technical and computational challenges inherent to these experimental methods, next-generation sequencing technologies are making such experiments accessible in any system with a sequenced genome. We further discuss the connection between copy-number variation within species and copy-number divergence between species, showing that these values are exactly what one would expect from similar comparisons of nucleotide polymorphism and divergence. We conclude by reviewing the growing body of evidence for natural selection on copy-number variants. While it appears that most genic CNVs—especially deletions—are quickly eliminated by selection, there are now multiple studies demonstrating a strong link between copy-number differences at specific genes and phenotypic differences in adaptive traits. We argue that a complete understanding of the molecular basis for adaptive natural selection necessarily includes the study of copy-number variation.     

Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster

A critical task in evolutionary genetics is to explain the persistence of heritable variation in fitness-related traits such as immunity. Ecological factors can maintain genetic variation in immunity, but less is known about the role of other factors, such as antagonistic pleiotropy, on immunity. Sexually dimorphic immunity—with females often being more immune-competent—may maintain variation in immunity in dioecious populations. Most eco-immunological studies assess host resistance to parasites rather than the host''s ability to maintain fitness during infection (tolerance). Distinguishing between resistance and tolerance is important as they are thought to have markedly different evolutionary and epidemiological outcomes. Few studies have investigated tolerance in animals, and the extent of sexual dimorphism in tolerance is unknown. Using males and females from 50 Drosophila melanogaster genotypes, we investigated possible sources of genetic variation for immunity by assessing both resistance and tolerance to the common bacterial pathogen Pseudomonas aeruginosa. We found evidence of sexual dimorphism and sexual antagonism for resistance and tolerance, and a trade-off between the two traits. Our findings suggest that antagonistic pleiotropy may be a major contributor to variation in immunity, with implications for host–parasite coevolution.     

Coevolutionary Constraints? The Environment Alters Tripartite Interaction Traits in a Legume

Third party species, which interact with one or both partners of a pairwise species interaction, can shift the ecological costs and the evolutionary trajectory of the focal interaction. Shared genes that mediate a host's interactions with multiple partners have the potential to generate evolutionary constraints, making multi-player interactions critical to our understanding of the evolution of key interaction traits. Using a field quantitative genetics approach, we studied phenotypic and genetic correlations among legume traits for rhizobium and herbivore interactions in two light environments. Shifts in plant biomass allocation mediated negative phenotypic correlations between symbiotic nodule number and herbivory in the field, whereas positive genetic covariances suggested shared genetic pathways between nodulation and herbivory response. Trait variance-covariance (G) matrices were not equal in sun and shade, but nevertheless responses to independent and correlated selection are expected to be similar in both environments. Interactions between plants and aboveground antagonists might alter the evolutionary potential of traits mediating belowground mutualisms (and vice versa). Thus our understanding of legume-rhizobium genetics and coevolution may be incomplete without a grasp of how these networks overlap with other plant interactions.     

Kin selection and the Evolution of Mutualisms between Species

Hamilton's theory of kin selection has revolutionized and inspired fifty years of additional theories and experiments on social evolution. Whereas Hamilton's broader intent was to explain the evolutionary stability of cooperation, his focus on shared genetic history appears to have limited the application of his theory to populations within a single species rather than across interacting species. The evolutionary mechanisms for cooperation between species require both spatial and temporal correlations among interacting partners for the benefits to be not only predictable but of sufficient duration to be reliably delivered. As a consequence when the benefits returned by mutualistic partners are redirected to individuals other than the original donor, cooperation usually becomes unstable and parasitism may evolve. However, theoretically, such redirection of mutualistic benefits may actually reinforce, rather than undermine, mutualisms between species when the recipients of these redirected benefits are genetically related to the original donor. Here, I review the few mathematical models that have used Hamilton's theory of kin selection to predict the evolution of mutualisms between species. I go on to examine the applicability of these models to the most well‐studied case of mutualism, pollinating seed predators, where the role of kin selection may have been previously overlooked. Future detailed studies of the direct, and indirect, benefits of mutualism are likely to reveal additional possibilities for applying Hamilton's theory of kin selection to mutualisms between species.     

Mutualism favours higher host specificity than does antagonism in plant–herbivore interaction

Coevolved mutualisms often exhibit high levels of partner specificity. Obligate pollination mutualisms, such as the fig–fig wasp and yucca–yucca moth systems, represent remarkable examples of such highly species-specific associations; however, the evolutionary processes underlying these patterns are poorly understood. The prevailing hypothesis suggests that the high degree of specificity in pollinating seed parasites is the fortuitous result of specialization in their ancestors because these insects are derived from endophytic herbivores that are themselves highly host-specific. Conversely, we show that in the Glochidion–Epicephala obligate pollination mutualism, pollinators are more host-specific than are closely related endophytic leaf-feeding taxa, which co-occur with Epicephala on the same Glochidion hosts. This difference is probably not because of shifts in larval diet (i.e. from leaf- to seed-feeding), because seed-eating lepidopterans other than Epicephala do not show the same degree of host specificity as Epicephala. Species of a tentative sister group of Epicephala each attack several distantly related plants, suggesting that the evolution of strict host specificity is tied to the evolution of pollinator habit. These results suggest that mutualists can attain higher host specificity than that of their parasitic ancestors and that coevolutionary selection can be a strong promoter of extreme reciprocal specialization in mutualisms.     

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.     

Proteases hold the key to an exclusive mutualism

Mutualisms, cooperative interactions between species, generally involve an economic exchange: species exchange commodities that are cheap for them to provide, for ones that cannot be obtained affordably or at all. But these associations can only succeed if effective partners can be enticed to interact. In some mutualisms, partners can actively seek one another out. However, plants, which use mutualists for a wide array of essential life history functions, do not have this option. Instead, natural selection has repeatedly favoured the evolution of rewards – nutritional substances (such as sugar‐rich nectar and fleshy fruit) with which plants attract certain organisms whose feeding activities can then be co‐opted for their own benefit. The trouble with rewards, however, is that they are usually also attractive to organisms that confer no benefits at all. Losing rewards to ‘exploiters’ makes a plant immediately less attractive to the mutualists it requires; if the reward cannot be renewed quickly (or at all), then mutualistic service is precluded entirely. Thus, it is in plants' interests to either restrict rewards to only the most beneficial partners or somehow punish or deter exploiters. Yet, at least in cases where the rewards are highly nutritious, we can expect counter‐selection for exploiter traits that permit them to skirt such control. How, then, can mutualisms persist? In this issue, Orona‐Tamayo et al. ( 2013 ) describe a remarkable adaptation that safeguards one particularly costly reward from nonmutualists. Their study helps to explain the evolutionary success of an iconic interaction and illuminates one way in which mutualism as a whole can persist in the face of exploitation.     

Experimental evidence of bark beetle adaptation to a fungal symbiont

The importance of symbiotic microbes to insects cannot be overstated; however, we have a poor understanding of the evolutionary processes that shape most insect–microbe interactions. Many bark beetle (Coleoptera: Curculionidae, Scolytinae) species are involved in what have been described as obligate mutualisms with symbiotic fungi. Beetles benefit through supplementing their nutrient‐poor diet with fungi and the fungi benefit through gaining transportation to resources. However, only a few beetle–fungal symbioses have been experimentally manipulated to test whether the relationship is obligate. Furthermore, none have tested for adaptation of beetles to their specific symbionts, one of the requirements for coevolution. We experimentally manipulated the western pine beetle–fungus symbiosis to determine whether the beetle is obligately dependent upon fungi and to test for fine‐scale adaptation of the beetle to one of its symbiotic fungi, Entomocorticium sp. B. We reared beetles from a single population with either a natal isolate of E. sp. B (isolated from the same population from which the beetles originated), a non‐natal isolate (a genetically divergent isolate from a geographically distant beetle population), or with no fungi. We found that fungi were crucial for the successful development of western pine beetles. We also found no significant difference in the effects of the natal and non‐natal isolate on beetle fitness parameters. However, brood adult beetles failed to incorporate the non‐natal fungus into their fungal transport structure (mycangium) indicating adaption by the beetle to particular genotypes of symbiotic fungi. Our results suggest that beetle–fungus mutualisms and symbiont fidelity may be maintained via an undescribed recognition mechanism of the beetles for particular symbionts that may promote particular associations through time.     

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.     

Evolutionary history shapes patterns of mutualistic benefit in Acacia–rhizobial interactions

The ecological and evolutionary factors that drive the emergence and maintenance of variation in mutualistic benefit (i.e., the benefits provided by one partner to another) in mutualistic symbioses are not well understood. In this study, we evaluated the role that host and symbiont phylogeny might play in determining patterns of mutualistic benefit for interactions among nine species of Acacia and 31 strains of nitrogen‐fixing rhizobial bacteria. Using phylogenetic comparative methods we compared patterns of variation in mutualistic benefit (host response to inoculation) to rhizobial phylogenies constructed from housekeeping and symbiosis genes; and a multigene host phylogeny. We found widespread genotype‐by‐genotype variation in patterns of plant growth. A relatively large component of this variation (21–28%) was strongly influenced by the interacting evolutionary histories of both partners, such that phylogenetically similar host species had similar growth responses when inoculated with phylogenetically similar rhizobia. We also found a relatively large nonphylogenetic effect for the average mutualistic benefit provided by rhizobia to plants, such that phylogenetic relatedness did not predict the overall benefit provided by rhizobia across all hosts. We conclude that phylogenetic relatedness should frequently predict patterns of mutualistic benefit in acacia‐rhizobial mutualistic interactions; but that some mutualistic traits also evolve independently of the phylogenies.