When mutualists are pathogens: an experimental study of the symbioses between Steinernema (entomopathogenic nematodes) and Xenorhabdus (bacteria)

In this paper, we investigate the level of specialization of the symbiotic association between an entomopathogenic nematode (Steinernema carpocapsae) and its mutualistic native bacterium (Xenorhabdus nematophila). We made experimental combinations on an insect host where nematodes were associated with non-native symbionts belonging to the same species as the native symbiont, to the same genus or even to a different genus of bacteria. All non-native strains are mutualistically associated with congeneric entomopathogenic nematode species in nature. We show that some of the non-native bacterial strains are pathogenic for S. carpocapsae. When the phylogenetic relationships between the bacterial strains was evaluated, we found a clear negative correlation between the effect a bacterium has on nematode fitness and its phylogenetic distance to the native bacteria of this nematode. Moreover, only symbionts that were phylogenetically closely related to the native bacterial strain were transmitted. These results suggest that co-evolution between the partners has led to a high level of specialization in this mutualism, which effectively prevents horizontal transmission. The pathogenicity of some non-native bacterial strains against S. carpocapsae could result from the incapacity of the nematode to resist specific virulence factors produced by these bacteria.     

Complex patterns of host switching in New World arenaviruses

We empirically tested the long-standing hypothesis of codivergence of New World arenaviruses (NWA) with their hosts. We constructed phylogenies for NWA and all known hosts and used them in reconciliation analyses. We also constructed a phylogenetic tree of all Sigmodontinae and Neotominae rodents and tested whether viral-host associations were phylogenetically clustered. We determined host geographical overlap to determine to what extent opportunity to switch hosts was limited by host relatedness or physical proximity. With the exception of viruses from North America, no phylogenetically codivergent pattern between NWA and their hosts was found. We found that different virus clades were clustered differently and that Clade B with members pathogenic to humans was randomly distributed across the rodent phylogeny. Furthermore, viral relatedness within Clade B was significantly explained by the geographic overlap of their hosts' ranges rather than host relatedness, indicating that they are capable of host switching opportunistically. This has important bearings on their potential to become panzootic. Together, these analyses suggest that NWA have not codiverged with their hosts and instead have evolved predominantly via host switching.     

A cophylogenetic perspective of RNA-virus evolution

The extent to which viruses and their hosts codiverge remains an open question, given that numerous cases of both "cospeciation" and horizontal switching have recently been documented. DNA viruses that form persistent infections are thought to be the most likely candidates for phylogenetic congruence. Phylogenetic reconciliation analysis was used to compare established phylogenies for four RNA viruses and their hosts. The analysis employs a cophylogeny mapping technique, implemented in TreeMap v2.0, to find the most parsimonious combinations of evolutionary events able to reconcile any incongruence. This technique is guaranteed to recover all potentially optimal solutions to the reconciled tree and specifically tests the null hypothesis that an associate phylogeny is no more congruent with a host phylogeny than would be a random tree with the same taxon set. Phylogenies for Hantavirus, Spumavirus, and avian sarcoma leukosis virus were found to be significantly similar to their host trees, whereas Lyssavirus and Arenavirus displayed no significant congruence. These results demonstrate that RNA viruses are able to form stable associations with their hosts over evolutionary time scales and that the details of such associations are consistent with persistent infection being a necessary but not sufficient precondition.     

蚜虫与其胞内共生细菌的相互作用

蚜虫—巴克纳氏菌之间是一种典型的互利共生关系,两者相互依存,缺少一方,另一方便不能生存。研究表明,共生细菌能为寄主蚜虫提供必需氨基酸和维生索,并对寄主具有一些非营养功能,如促进蚜虫传播循环性病毒等。寄主蚜虫则是为共生菌提供一个合适的生存场所,并对共生菌的生长和繁殖进行调控。现代分子生物学技术从基因水平证明了蚜虫与共生菌的相互依赖性。     

Co‐evolution of marine worms and their chemoautotrophic bacterial symbionts: unexpected host switches explained by ecological fitting?

Mutualistic associations of bacteria and invertebrates are widespread and encompass an enormous diversity on the side of both partners. The advantages gained from the symbiosis favour reciprocal adaptations that increase the stability of the association and can lead to codiversification of symbiont and host. While numerous examples of a strictly vertical transfer of the symbionts from parent to offspring among intracellular associations abound, little is known about the fidelity of the partners in extracellular associations, where symbionts colonize the surface or body cavity of their host. In this issue of Molecular Ecology, Zimmermann et al. ( 2016 ) investigated the evolutionary history of the symbiotic association between a monophyletic clade of sulphur‐oxidizing Gammaproteobacteria and two distantly related lineages of marine worms (nematodes and annelids). The study supports the surprising conclusion that partner fidelity does not necessarily increase with the intimacy of the association. Ectosymbionts on the cuticle of the nematodes seem to be cospeciating with their hosts, whereas endosymbionts housed in the body cavity of the annelids must have originated multiple times, probably by host switching, from ectosymbionts of sympatric nematodes. This excellent case study on the evolutionary history of invertebrate–microbe interactions supports the emerging concept that the co‐evolutionary processes shaping such mutualistic symbioses include both codiversification and ecological fitting.     

Endophytic fungi reduce leaf-cutting ant damage to seedlings

Our study examines how the mutualism between Atta colombica leaf-cutting ants and their cultivated fungus is influenced by the presence of diverse foliar endophytic fungi (endophytes) at high densities in tropical leaf tissues. We conducted laboratory choice trials in which ant colonies chose between Cordia alliodora seedlings with high (E_high) or low (E_low) densities of endophytes. The E_high seedlings contained 5.5 times higher endophyte content and a greater diversity of fungal morphospecies than the E_low treatment, and endophyte content was not correlated with leaf toughness or thickness. Leaf-cutting ants cut over 2.5 times the leaf area from E_low relative to E_high seedlings and had a tendency to recruit more ants to E_low plants. Our findings suggest that leaf-cutting ants may incur costs from cutting and processing leaves with high endophyte loads, which could impact Neotropical forests by causing variable damage rates within plant communities.     

Breakdown and delayed cospeciation in the arbuscular mycorrhizal mutualism

The ancient arbuscular mycorrhizal association between the vast majority of plants and the fungal phylum Glomeromycota is a dominant nutritional mutualism worldwide. In the mycorrhizal mutualism, plants exchange photosynthesized carbohydrates for mineral nutrients acquired by fungi from the soil. This widespread cooperative arrangement is broken by 'cheater' plant species that lack the ability to photosynthesize and thus become dependent upon three-partite linkages (cheater-fungus-photosynthetic plant). Using the first fine-level coevolutionary analysis of mycorrhizas, we show that extreme fidelity towards fungi has led cheater plants to lengthy evolutionary codiversification. Remarkably, the plants' evolutionary history closely mirrors that of their considerably older mycorrhizal fungi. This demonstrates that one of the most diffuse mutualistic networks is vulnerable to the emergence, persistence and speciation of highly specific cheaters.     

On the evolution of non-specific mutualism

It has been argued that mutualisms are non-specific when mutualistic interactions are weak and transient, and become more specific as interactions increase in strength. However, this runs counter to the observation that there exist tightly linked mutualisms of great antiquity that are highly nonspecific. Here we argue that mutualism generates positive, interspecific, frequency-dependent selection, which acts as a cohesive evolutionary force, discouraging evolution of specificity. A simple mathematical model is constructed to analyse the evolution of a community consisting of two guilds of species with mutualistic between-guild interactions, two competing species in each guild and two genetically distinct phenotypes within each species. With some simplifying assumptions, the trajectories in the neighbourhood of the only interior equilibrium point are determined analytically in terms of interactions between individuals. These show that the equilibrium is locally stable (no evolution) when there is little differentiation between phenotypes in mutualistic and interspecific, competitive interactions. On the other hand, when there is strong differentiation between phenotypes in their mutualistic interactions, the equilibrium is unstable and the community starts to evolve towards non-specificity. There are, however, two forces counteracting this tendency which, if sufficiently potent, cause evolution towards specificity. The first is generated by strong differentiation between phenotypes in interspecific competition; the second is caused by specificity which already exists between species in their mutualistic interactions. Thus, the tendency for non-specificity or specificity to evolve depends on the interplay between antagonistic and mutualistic interactions in the community. We illustrate these results with some numerical examples and, finally, survey some data on specificity of mutualisms in the light of the analysis.     

Phylogeny and fitness of Vibrio fischeri from the light organs of Euprymna scolopes in two Oahu,Hawaii populations

The evolutionary relationship among Vibrio fischeri isolates obtained from the light organs of Euprymna scolopes collected around Oahu, Hawaii, were examined in this study. Phylogenetic reconstructions based on a concatenation of fragments of four housekeeping loci (recA, mdh, katA, pyrC) identified one monophyletic group (‘Group-A'') of V. fischeri from Oahu. Group-A V. fischeri strains could also be identified by a single DNA fingerprint type. V. fischeri strains with this fingerprint type had been observed to be at a significantly higher abundance than other strains in the light organs of adult squid collected from Maunalua Bay, Oahu, in 2005. We hypothesized that these previous observations might be related to a growth/survival advantage of the Group-A strains in the Maunalua Bay environments. Competition experiments between Group-A strains and non-Group-A strains demonstrated an advantage of the former in colonizing juvenile Maunalua Bay hosts. Growth and survival assays in Maunalua Bay seawater microcosms revealed a reduced fitness of Group-A strains relative to non-Group-A strains. From these results, we hypothesize that there may exist trade-offs between growth in the light organ and in seawater environments for local V. fischeri strains from Oahu. Alternatively, Group-A V. fischeri may represent an example of rapid, evolutionarily significant, specialization of a horizontally transmitted symbiont to a local host population.     

Biotic environments and the maintenance of sex–some evidence from mutualistic symbioses

It has previously been proposed that sex is selected for in organisms living in antagonistic biotic environments. Here, the contrasting case of mutualistic biotic environments is considered. In these environments, it is argued that there should be selection against sex and an accompanying low rate of genetic change. This proposition is tested on mutualistic symbioses with substantial histories of co-evolution in which one partner, the inhabitant, lives partly or wholly inside the other, the exhabitant. This asymmetry between the partners means that inhabitants should exhibit a reduction in sex in comparison to related free-living taxa and a lower rate of genetic change than exhabitants.
The patterns that emerge from an analysis of 10 kinds of mutualistic symbiosis strongly support these predictions. Where adequate information is available, sex is usually reduced in inhabitants in comparison to related free-living taxa, although it remains widespread in exhabitants. Inhabitants are also represented by a much smaller taxonomic diversity than exhabitants. Various alternative reasons for these patterns are considered but it is concluded that they are best explained by the mutualistic environment in which the inhabitants live.