Costs,benefits, and loss of vertically transmitted symbionts affect host population dynamics

The costs and benefits of symbiotic interactions may vary with host and symbiont ontogeny. Effects of symbionts at different stages of host development or on different host demographic rates do not contribute equally to fitness. Although rarely applied, a population dynamics approach that integrates over the host life cycle is therefore necessary for capturing the net costs or benefits and, thus, the mutualistic or parasitic nature of symbioses. Using the native, disturbance‐specialist grass Agrostis hyemalis, we asked how a symbiotic endophyte affected the population dynamics of its host and how imperfect vertical transmission influenced symbiont frequency in a late successional environment. A size‐structured integral projection model (IPM) parameterized with experimental field data showed that greater rates of individual growth and reproduction for endophyte‐symbiotic (E+) hosts outweighed their lower rates of survival, leading to a net positive effect of symbiosis on equilibrium plant population growth (slower rate of extinction). Given that populations under going successional transitions are unlikely to be at an equilibrium size structure, we also conducted transient analysis that showed an initial short‐term cost to endophyte symbiosis. We used a megamatrix approach to link E? and E+ IPMs via imperfect vertical transmission and found that this parameter strongly influenced the frequency of symbiosis via complex interactions with host demographic rates. Overall, our population dynamics approach improves the ability to characterize the outcome of symbiotic interactions, and results suggest that particular attention should be paid to interactions between the rate of vertical transmission and host demography.     

A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum

One of the outstanding and poorly understood examples of cooperation between species is found in corals, hydras and jellyfish that form symbioses with algae. These mutualistic algae are mostly acquired infectiously from the seawater and, according to models of virulence evolution, should be selected to parasitize their hosts. We altered algal transmission between jellyfish hosts in the laboratory to examine the potential for virulence evolution in this widespread symbiosis. In one experimental treatment, vertical transmission of algae (parent to offspring) selected for symbiont cooperation, because symbiont fitness was tied to host reproduction. In the other treatment, horizontal transmission (infectious spread) decoupled symbiont fitness from the host, potentially allowing parasitic symbionts to spread. Fitness estimates revealed a striking shift to parasitism in the horizontal treatment. The horizontally transmitted algae proliferated faster within hosts and had higher dispersal rates from hosts compared to the vertical treatment, while reducing host reproduction and growth. However, a trade-off was detected between harm caused to hosts and symbiont fitness. Virulence trade-offs have been modelled for pathogens and may be critical in stabilising 'infectious' symbioses. Our results demonstrate the dynamic nature of this symbiosis and illustrate the potential ease with which beneficial symbionts can evolve into parasites.     

Evolution of Mutualistic Symbiosis without Vertical Transmission

Mutualistic symbioses are considered to evolve from parasitic relationships. Vertical transmission, defined as the direct transfer of infection from a parent organism to its progeny, has been suggested as a key factor causing reduction of symbiont virulence and evolution of mutualism. On the other hand, there are several mutualistic associations without vertical transmission, such as those between plants and mycorrhizal fungi, legumes and rhizobia, and some corals and dinoflagellates. It is expected that all mutualisms evolve perfect vertical transmission if the relationship is really mutualistic, because hosts may fail to acquire symbionts if they do not transmit the symbionts by vertical transmission. We have developed a mathematical model to clarify the conditions under which mutualistic symbiosis without vertical transmission should evolve. The evolution may occur when and only when (i) vertical transmission involves some costs in the host, (ii) the symbiont suffers direct negative effects if it exploits the host too intensively, (iii) the host establishes the ability to make use of waste products from the symbiont, and (iv) the mechanism of vertical transmission is controlled by the host. We also clarify the conditions under which mutualistic symbiosis with vertical transmission evolves.     

Symbiosis lost: imperfect vertical transmission of fungal endophytes in grasses

Vertically transmitted symbionts associate with some of the most ecologically dominant species on Earth, and their fixation has led to major evolutionary transitions (e.g., the development of mitochondria). Theory predicts that exclusive vertical transmission should favor mutualism and generate high frequencies of symbiosis in host populations. However, host populations often support lower-than-expected symbiont frequencies. Imperfect transmission (i.e., symbiont is not transmitted to all offspring) can reduce symbiont frequency, but for most beneficial symbionts it is unknown whether vertical transmission can be imperfect or during which life-history stage the symbiont is lost. Using quantitative natural history surveys of fungal endophytes in grasses, we show that transmission was imperfect in at least one stage for all seven host species examined. Endophytes were lost at all possible stages: within adult plants, from adult tillers to seeds, and from seeds to seedlings. Despite this loss, uninfected seeds failed to germinate in some species, resulting in perfect transmission to seedlings. The type and degree of loss differed among host populations and species and between endophyte genera. Populations with lower endophyte frequencies had higher rates of loss. Our results indicate new directions for understanding cooperation and conflict in symbioses and suggest mechanisms for host sanctions against costly symbionts.     

A novel test for host-symbiont codivergence indicates ancient origin of fungal endophytes in grasses

Significant phylogenetic codivergence between plant or animal hosts (H) and their symbionts or parasites (P) indicates the importance of their interactions on evolutionary time scales. However, valid and realistic methods to test for codivergence are not fully developed. One of the systems where possible codivergence has been of interest involves the large subfamily of temperate grasses (Pooideae) and their endophytic fungi (epichloae). These widespread symbioses often help protect host plants from herbivory and stresses and affect species diversity and food web structures. Here we introduce the MRCALink (most-recent-common-ancestor link) method and use it to investigate the possibility of grass-epichlo? codivergence. MRCALink applied to ultrametric H and P trees identifies all corresponding nodes for pairwise comparisons of MRCA ages. The result is compared to the space of random H and P tree pairs estimated by a Monte Carlo method. Compared to tree reconciliation, the method is less dependent on tree topologies (which often can be misleading), and it crucially improves on phylogeny-independent methods such as ParaFit or the Mantel test by eliminating an extreme (but previously unrecognized) distortion of node-pair sampling. Analysis of 26 grass species-epichlo? species symbioses did not reject random association of H and P MRCA ages. However, when five obvious host jumps were removed, the analysis significantly rejected random association and supported grass-endophyte codivergence. Interestingly, early cladogenesis events in the Pooideae corresponded to early cladogenesis events in epichloae, suggesting concomitant origins of this grass subfamily and its remarkable group of symbionts. We also applied our method to the well-known gopher-louse data set.     

A gene's-eye view of symbiont transmission

Symbiotic associations between species are ubiquitous, but we only poorly understand why some symbioses evolve to be mutualistic and others to be parasitic. One prominent hypothesis holds that vertical transmission of symbionts from host parents to their offspring selects for symbionts that are benign or beneficial, while horizontal transmission of symbionts among unrelated hosts selects for symbionts that are less beneficial or outright harmful. A long-standing challenge to this hypothesis, however, is the existence of selfish genetic elements (SGEs). SGEs are passed exclusively from parent to offspring and are able to spread and persist in populations despite reducing the fitness of their hosts. Here I show that SGEs are in fact consistent with the transmission mode hypothesis if one measures transmission from the perspective of host genes instead of host organisms. Both meiotic drive genes and cytoplasmic sex ratio distorters require horizontal transmission, in the form of outbred sex, to spread as parasites. Transmission from parent to offpsring does not constrain SGEs to evolve toward mutualism. The gene-centered perspective I present here is applicable to symbioses at all levels of selection and brings closer together our understandings of cooperation within and between species.     

An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects

Across animals and plants, numerous metabolic and defensive adaptations are a direct consequence of symbiotic associations with beneficial microbes. Explaining how these partnerships are maintained through evolutionary time remains one of the central challenges within the field of symbiosis research. While genome erosion and co-cladogenesis with the host are well-established features of symbionts exhibiting intracellular localization and transmission, the ecological and evolutionary consequences of an extracellular lifestyle have received little attention, despite a demonstrated prevalence and functional importance across many host taxa. Using insect–bacteria symbioses as a model, we highlight the diverse routes of extracellular symbiont transfer. Extracellular transmission routes are unified by the common ability of the bacterial partners to survive outside their hosts, thereby imposing different genomic, metabolic and morphological constraints than would be expected from a strictly intracellular lifestyle. We emphasize that the evolutionary implications of symbiont transmission routes (intracellular versus extracellular) do not necessarily correspond to those of the transmission mode (vertical versus horizontal), a distinction of vital significance when addressing the genomic and physiological consequences for both host and symbiont.     

Evolution of transmission mode in conditional mutualisms with spatial variation in symbiont quality

Many symbioses have costs and benefits to their hosts that vary with the environmental context, which itself may vary in space. The same symbiont may be a mutualist in one location and a parasite in another. Such spatially conditional mutualisms pose a dilemma for hosts, who might evolve (higher or lower) horizontal or vertical transmission to increase their chances of being infected only where the symbiont is beneficial. To determine how transmission in hosts might evolve, we modeled transmission evolution where the symbiont had a spatially conditional effect on either host lifespan or fecundity. We found that over ecological time, symbionts that affected lifespan but not fecundity led to high frequencies of infected hosts in areas where the symbiont was beneficial and low frequencies elsewhere. In response, hosts evolved increased horizontal transmission only when the symbiont affected lifespan. We also modeled transmission evolution in symbionts, which evolved high horizontal and vertical transmission, indicating a possible host–symbiont conflict over transmission mode. Our results suggest an eco‐evolutionary feedback where the component of host fitness affected by a conditionally mutualistic symbiont in turn determines its distribution in the population, and, through this, the transmission mode that evolves.     

Interplay between Endophyte Prevalence,Effects and Transmission: Insights from a Natural Grass Population

Two main mechanisms are thought to affect the prevalence of endophyte-grass symbiosis in host populations: the mode of endophyte transmission, and the fitness differential between symbiotic and non-symbiotic plants. These mechanisms have mostly been studied in synthetic grass populations. If we are to improve our understanding of the ecological and evolutionary dynamics of such symbioses, we now need to determine the combinations of mechanisms actually operating in the wild, in populations shaped by evolutionary history. We used a demographic population modeling approach to identify the mechanisms operating in a natural stand of an intermediate population (i.e. 50% of plants symbiotic) of the native grass Festuca eskia. We recorded demographic data in the wild over a period of three years, with manipulation of the soil resources for half the population. We developed two stage-structured matrix population models. The first model concerned either symbiotic or non-symbiotic plants. The second model included both symbiotic and non-symbiotic plants and took endophyte transmission rates into account. According to our models, symbiotic had a significantly higher population growth rate than non-symbiotic plants, and endophyte prevalence was about 58%. Endophyte transmission rates were about 0.67 or 0.87, depending on the growth stage considered. In the presence of nutrient supplementation, population growth rates were still significantly higher for symbiotic than for non-symbiotic plants, but endophyte prevalence fell to 0%. At vertical transmission rates below 0.10–0.20, no symbiosis was observed. Our models showed that a positive benefit of the endophyte and vertical transmission rates of about 0.6 could lead to the coexistence of symbiotic and non-symbiotic F. eskia plants. The positive effect of the symbiont on host is not systematically associated with high transmission rates of the symbiont over short time scales, in particular following an environmental change.     

Convergent evolution of the vertical transmission mode of the cyanobacterial obligate symbiont Prochloron distributed in the tunic of colonial ascidians

In chordates, obligate photosynthetic symbiosis has been reported exclusively in some colonial ascidians of the family Didemnidae. The vertical transmission of the symbionts is crucial in establishing the obligate symbiosis between the cyanobacteria and the host ascidians. The results of comparative surveys on the morphological processes of cyanobacterial transmission suggest the occurrence of convergent evolution of the vertical transmission in the host species harboring symbionts in the cloacal cavity. In Trididemnum species harboring cyanobacterial cells in the tunic, the symbiont cells are transported by the tunic cells to the tunic of embryos brooded in the tunic of the parent colony. The present study examined whether the mode of symbiont transmission is the same in host species harboring the symbionts in the tunic, regardless of host genera, or whether non-Trididemnum hosts have a different vertical transmission mode. Our results showed that the vertical transmission process in Lissoclinum midui was almost the same as in the Trididemnum species, supporting the occurrence of convergent evolution in the two distinct didemnid genera, that is, Trididemnum and Lissoclinum. High plasticity of the embryogenic process in didemnid ascidians may be important in developing the mechanism of vertical transmission; this assumption may also explain why the obligate cyanobacterial symbiosis has been exclusively established in didemnid ascidians among chordates.     

An ecological cost associated with protective symbionts of aphids

Beneficial symbioses are widespread and diverse in the functions they provide to the host ranging from nutrition to protection. However, these partnerships with symbionts can be costly for the host. Such costs, so called “direct costs”, arise from a trade‐off between allocating resources to symbiosis and other functions such as reproduction or growth. Ecological costs may also exist when symbiosis negatively affects the interactions between the host and other organisms in the environment. Although ecological costs can deeply impact the evolution of symbiosis, they have received little attention. The pea aphid Acyrthosiphon pisum benefits a strong protection against its main parasitoids from protective bacterial symbionts. The ecological cost of symbiont‐mediated resistance to parasitism in aphids was here investigated by analyzing aphid behavior in the presence of predatory ladybirds. We showed that aphids harboring protective symbionts expressed less defensive behaviors, thus suffering a higher predation than symbiont‐free aphids. Consequently, our study indicates that this underlined ecological cost may affect both the coevolutionary processes between symbiotic partners and the prevalence of such beneficial bacterial symbionts in host natural populations.     

The impact of transmission mode on the evolution of benefits provided by microbial symbionts

While past work has often examined the effects of transmission mode on virulence evolution in parasites, few studies have explored the impact of horizontal transmission on the evolution of benefits conferred by a symbiont to its host. Here, we identify three mechanisms that create a positive covariance between horizontal transmission and symbiont‐provided benefits: pleiotropy within the symbiont genome, partner choice by the host, and consumption of host waste by‐products by symbionts. We modify a susceptible‐infected model to incorporate the details of each mechanism and examine the evolution of symbiont benefits given variation in either the immigration rate of susceptible hosts or the rate of successful vertical transmission. We find conditions for each case under which greater opportunity for horizontal transmission (higher migration rate) favors the evolution of mutualism. Further, we find the surprising result that vertical transmission can inhibit the evolution of benefits provided by symbionts to hosts when horizontal transmission and symbiont‐provided benefits are positively correlated. These predictions may apply to a number of natural systems, and the results may explain why many mutualisms that rely on partner choice often lack a mechanism for vertical transmission.     

Does host outcrossing disrupt compatibility with heritable symbionts?

Vertically transmitted microbes are common in macro‐organisms and can enhance host defense against environmental stress. Because vertical transmission couples host and symbiont lineages, symbionts may become specialized to host species or genotypes. Specialization and contrasting reproductive modes of symbiotic partners could create incompatibilities between inherited symbionts and novel host genotypes when hosts outcross or hybridize. Such incompatibilities could manifest as failed colonization or poor symbiont growth in host offspring that are genetically dissimilar from their maternal host. Moreover, outcrossing between host species could influence both host and symbiont reproductive performance. We tested these hypotheses by manipulating outcrossing between populations and species of two grasses, Elymus virginicus and E. canadensis, that host vertically transmitted fungal endophytes (genus Epichloё). In both greenhouse and field settings, we found that host–symbiont compatibility was robust to variation in host genetic background, spanning within‐population, between‐population and between‐species crosses. Symbiont transmission into the F₁ generation was generally high and weakly affected by host outcrossing. Furthermore, endophytes grew equally well in planta regardless of host genetic background and transmitted at high frequencies into the F₂ generation. However, outcrossing, especially inter‐specific hybridization, reduced reproductive fitness of the host, and thereby the symbiont. Our results challenge the hypothesis that host genetic recombination, which typically exceeds that of symbionts, is a disruptive force in heritable symbioses. Instead, symbionts may be sufficiently generalized to tolerate ecologically realistic variation in host outcrossing.     

Symbiogenesis as Evolution of Open Genetic Systems

The evolution of intracellular symbioses formed by bacteria with plants and animals is addressed as a model for reconstructing the origin of eukaryotic cells as a symbiosis between different forms of prokaryotes (symbiogenesis). In microorganisms that are in facultative or conditionally obligatory (ecologically obligatory) dependence on symbiosis, their gene networks arise on the basis of host-activated intragenomic rearrangements and horizontal gene transfer. The latter factor determines the evolution of the genomes of symbiotic bacteria as open genetic systems (OGSs), in which the ratio of accessory genome regions to its core regions is increased compared to free-living relatives. Coevolution of bacteria and eukaryotic hosts results in the formation of higher rank OGSs, symbiogenomes, the integrity of which is mediated by signaling interactions that determine cross-regulation of partner genes. Increasing the effectiveness of their cooperation is achieved with the transition of bacteria to strictly obligatory (genetically obligatory) dependence on hosts, determined by (a) the loss of considerable regions of the microbial genome encoding the functions of autonomous development and (b) adaptation of bacteria to permanent intracellular existence, endocytobiosis. At this stage, symbiogenomes acquire the status of inheritance systems, determined by vertical (as a rule, transovarial) transfer of microsymbionts through host generations. The transformation of endocytobionts into cellular organelles is associated with the loss of their genetic autonomy, i.e., the ability to maintain and express their rudimentary genomes, until their complete loss. However, organelles partially retain phenotypic identity of ancestral bacteria, which is determined by the importation from the host cell of the gene products (proteins, RNA) obtained earlier from microsymbionts, which led to the formation of structurally integrated hologenomes. The gene loss and gain strategy realized in this way led to the formation of different patterns of eukaryotic cell organization in accordance with the mosaic scenario, which includes sequential introduction of several symbionts into the host cell, or with the matryoshka doll scenario, in which new symbionts are introduced into the cells of previously acquired symbionts.     

Water availability alters the tri-trophic consequences of a plant-fungal symbiosis

Plant–microbe protection symbioses occur when a symbiont defends its host against enemies (e.g., insect herbivores); these interactions can have important influences on arthropod abundance and composition. Understanding factors that generate context-dependency in protection symbioses will improve predictions on when and where symbionts are most likely to affect the ecology and evolution of host species and their associated communities. Of particular relevance are changes in abiotic contexts that are projected to accompany global warming. For example, increased drought stress can enhance the benefits of fungal symbiosis in plants, which may have multi-trophic consequences for plant-associated arthropods. Here, we tracked colonization of fungal endophyte-symbiotic and aposymbiotic Poa autumnalis (autumn bluegrass) by Rhopalosiphum padi (bird-cherry-oat aphids) and their parasitoids (Aphelinus sp.) following manipulations of soil water levels. Endophyte symbiosis significantly reduced plant colonization by aphids. Under low water, symbiotic plants also supported a significantly higher proportion of aphids that were parasitized by Aphelinus and had higher above-ground biomass than aposymbiotic plants, but these endophyte-mediated effects disappeared under high water. Thus, the multi-trophic consequences of plant-endophyte symbiosis were contingent on the abiotic context, suggesting the potential for complex responses in the arthropod community under future climate shifts.     

Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host

Members of several bacterial lineages are known only as symbionts of insects and move among hosts through maternal transmission. Such vertical transfer promotes strong fidelity within these associations, favoring the evolution of microbially mediated effects that improve host fitness. However, phylogenetic evidence indicates occasional horizontal transfer among different insect species, suggesting that some microbial symbionts retain a generalized ability to infect multiple hosts. Here we examine the abilities of three vertically transmitted bacteria from the Gammaproteobacteria to infect and spread within a novel host species, the pea aphid, Acyrthosiphon pisum. Using microinjection, we transferred symbionts from three species of natural aphid hosts into a common host background, comparing transmission efficiencies between novel symbionts and those naturally infecting A. pisum. We also examined the fitness effects of two novel symbionts to determine whether they should persist under natural selection acting at the host level. Our results reveal that these heritable bacteria vary in their capacities to utilize A. pisum as a host. One of three novel symbionts failed to undergo efficient maternal transmission in A. pisum, and one of the two efficiently transmitted bacteria depressed aphid growth rates. Although these findings reveal that negative fitness effects and low transmission efficiency can prevent the establishment of a new infection following horizontal transmission, they also indicate that some symbionts can overcome these obstacles, accounting for their widespread distributions across aphids and related insects.     

Transmission,relatedness, and the evolution of cooperative symbionts

Cooperative interactions between species, termed mutualisms, play a key role in shaping natural ecosystems, economically important agricultural systems, and in influencing human health. Across different mutualisms, there is significant variation in the benefit that hosts receive from their symbionts. Empirical data suggest that transmission mode can help explain this variation: vertical transmission, where symbionts infect their host's offspring, leads to symbionts that provide greater benefits to their hosts than horizontal transmission, where symbionts leave their host and infect other hosts in the population. However, two different theoretical explanations have been given for this pattern: firstly, vertical transmission aligns the fitness interests of hosts and their symbionts; secondly, vertical transmission leads to increased relatedness between symbionts sharing a host, favouring cooperation between symbionts. We used a combination of analytical models and dynamic simulations to tease these factors apart, in order to compare their separate influences and see how they interact. We found that relatedness between symbionts sharing a host, rather than transmission mode per se, was the most important factor driving symbiont cooperation. Transmission mode mattered mainly because it determined relatedness. We also found evolutionary branching throughout much of our simulation, suggesting that a combination of transmission mode and multiplicity of infections could lead to the stable coexistence of different symbiont strategies.     

Can maternally inherited endosymbionts adapt to a novel host? Direct costs of Spiroplasma infection,but not vertical transmission efficiency,evolve rapidly after horizontal transfer into D. melanogaster

Maternally inherited symbionts are common in arthropods and many have important roles in host adaptation. The observation that specific symbiont lineages infect distantly related host species implies new interactions are commonly established by lateral transfer events. However, studies have shown that symbionts often perform poorly in novel hosts. We hypothesized selection on the symbiont may be sufficiently rapid that poor performance in a novel host environment is rapidly ameliorated, permitting symbiont maintenance. Here, we test this prediction for a Spiroplasma strain transinfected into the novel host Drosophila melanogaster. In the generations immediately following transinfection, the symbiont had low transmission efficiency to offspring and imposed severe fitness costs on its host. We observed that effects on host fitness evolved rapidly, being undetectable after 17 generations in the novel host, whereas vertical transmission efficiency was poorly responsive over this period. Our results suggest that long-term symbiosis may more readily be established in cases where symbionts perform poorly in just one aspect of symbiosis.     

Horizontal Transfer of Bacterial Symbionts: Heritability and Fitness Effects in a Novel Aphid Host

Members of several bacterial lineages are known only as symbionts of insects and move among hosts through maternal transmission. Such vertical transfer promotes strong fidelity within these associations, favoring the evolution of microbially mediated effects that improve host fitness. However, phylogenetic evidence indicates occasional horizontal transfer among different insect species, suggesting that some microbial symbionts retain a generalized ability to infect multiple hosts. Here we examine the abilities of three vertically transmitted bacteria from the Gammaproteobacteria to infect and spread within a novel host species, the pea aphid, Acyrthosiphon pisum. Using microinjection, we transferred symbionts from three species of natural aphid hosts into a common host background, comparing transmission efficiencies between novel symbionts and those naturally infecting A. pisum. We also examined the fitness effects of two novel symbionts to determine whether they should persist under natural selection acting at the host level. Our results reveal that these heritable bacteria vary in their capacities to utilize A. pisum as a host. One of three novel symbionts failed to undergo efficient maternal transmission in A. pisum, and one of the two efficiently transmitted bacteria depressed aphid growth rates. Although these findings reveal that negative fitness effects and low transmission efficiency can prevent the establishment of a new infection following horizontal transmission, they also indicate that some symbionts can overcome these obstacles, accounting for their widespread distributions across aphids and related insects.