Incorporating the process of vertical transmission into understanding of host–symbiont dynamics

Variation exists in the frequency of obligate, vertically transmitted symbiotic organisms within and among host populations; however, these patterns have not been adequately explained by variable fitness effects of symbionts on their hosts. In this forum, we call attention to another equally important, but overlooked mechanism to maintain variation in the frequency of symbioses in nature: the rate of vertical transmission. On ecological time scales, vertical transmission can affect the equilibrium frequencies of symbionts in host populations, with potential consequences for population and community dynamics. In addition, vertical transmission has the potential to influence the evolution of symbiosis, by affecting the probability of fixation of symbiosis (and therefore the evolution of complexity) and by allowing hosts to sanction against costly symbionts. Here we use grass–epichloae symbioses as a model system to explore the causes and consequences of variation in vertical transmission rates. We identify critical points for symbiont transmission that emerge from considering the host growth cycle devoted to reproduction (asexual vs sexual) and the host capability to maintain homeostasis. We also use information on the process of transmission to predict the environmental factors that would most likely affect transmission rates. Altogether, we aim to highlight the vertical transmission rate as an important process for understanding the ecology and evolution of symbiosis, using grass–epichloae interactions as a case study.     

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.     

TRADEOFF BETWEEN HORIZONTAL AND VERTICAL MODES OF TRANSMISSION IN BACTERIAL PLASMIDS

It has been hypothesized that there is a fundamental conflict between horizontal (infectious) and vertical (intergenerational) modes of parasite transmission. Activities of a parasite that increase its rate of infectious transmission are presumed to reduce its host's fitness. This reduction in host fitness impedes vertical transmission of the parasite and causes a tradeoff between horizontal and vertical transmission. Given this tradeoff, and assuming no multiple infections (no within-host competition among parasites), a simple model predicts that the density of uninfected hosts in the environment should determine the optimum balance between modes of parasite transmission. When susceptible hosts are abundant, selection should favor increased rates of horizontal transfer, even at the expense of reduced vertical transmission. Conversely, when hosts are rare, selection should favor increased vertical transmission even at the expense of lower horizontal transfer. We tested the tradeoff hypothesis and these evolutionary predictions using conjugative plasmids and the bacteria that they infect. Plasmids were allowed to evolve for 500 generations in environments with different densities of susceptible hosts. The plasmid's rate of horizontal transfer by conjugation increased at the expense of host fitness, indicating a tradeoff between horizontal and vertical transmission. Also, reductions in conjugation rate repeatedly coincided with the loss of a particular plasmid-encoded antibiotic resistance gene. However, susceptible host density had no significant effect on the evolution of horizontal versus vertical modes of plasmid transmission. We consider several possible explanations for the failure to observe such an effect.     

Evolutionary double suicide in symbiotic systems

Mutualism is thought to face a threat of coextinction cascade because the loss of a member species could lead to the extinction of the other member. Despite this common emphasis on the perils of such knock-on effect, hitherto, the evolutionary causes leading to extinction have been less emphasised. Here, we examine how extinction could be triggered in mutualism and whether an evolutionary response to partner loss could prevent collateral extinctions, by theoretically examining the coevolution of the host exploitation by symbionts and host dependence on symbiosis. Our model reveals that mutualism is more vulnerable to co-extinction through adaptive evolution (evolutionary double suicide) than parasitism. Additionally, it shows that the risk of evolutionary double suicide rarely promotes the backward evolution to an autonomous (non-symbiotic) state. Our results provide a new perspective on the evolutionary fragility of mutualism and the rarity of observed evolutionary transitions from mutualism to parasitism.     

DYNAMIC TRANSMISSION,HOST QUALITY,AND POPULATION STRUCTURE IN A MULTIHOST PARASITE OF BUMBLEBEES

The evolutionary ecology of multihost parasites is predicted to depend upon patterns of host quality and the dynamics of transmission networks. Depending upon the differences in host quality and transmission asymmetries, as well as the balance between intra‐ and interspecific transmission, the evolution of specialist or generalist strategies is predicted. Using a trypanosome parasite of bumblebees, we ask how host quality and transmission networks relate to parasite population structure across host species, and thus the potential for the evolution of specialist strains adapted to different host species. Host species differed in quality, with parasite growth varying across host species. Highly asymmetric transmission networks, together with differences in host quality, likely explain local population structure of the parasite across host species. However, parasite population structure across years was highly dynamic, with parasite populations varying significantly from one year to the next within individual species at a given site. This suggests that, while host quality and transmission may provide the opportunity for short‐term host specialization by the parasite, repeated bottlenecking of the parasite, in combination with its own reproductive biology, overrides these smaller scale effects, resulting in the evolution of a generalist parasite.     

Parasitism,the diversity of life,and paleoparasitology

The parasite-host-environment system is dynamic, with several points of equilibrium. This makes it difficult to trace the thresholds between benefit and damage, and therefore, the definitions of commensalism, mutualism, and symbiosis become worthless. Therefore, the same concept of parasitism may encompass commensalism, mutualism, and symbiosis. Parasitism is essential for life. Life emerged as a consequence of parasitism at the molecular level, and intracellular parasitism created evolutive events that allowed species to diversify. An ecological and evolutive approach to the study of parasitism is presented here. Studies of the origin and evolution of parasitism have new perspectives with the development of molecular paleoparasitology, by which ancient parasite and host genomes can be recovered from disappeared populations. Molecular paleoparasitology points to host-parasite co-evolutive mechanisms of evolution traceable through genome retrospective studies.     

The evolution of reduced antagonism—A role for host–parasite coevolution

Why do some host–parasite interactions become less antagonistic over evolutionary time? Vertical transmission can select for reduced antagonism. Vertical transmission also promotes coevolution between hosts and parasites. Therefore, we hypothesized that coevolution itself may underlie transitions to reduced antagonism. To test the coevolution hypothesis, we selected for reduced antagonism between the host Caenorhabditis elegans and its parasite Serratia marcescens. This parasite is horizontally transmitted, which allowed us to study coevolution independently of vertical transmission. After 20 generations, we observed a response to selection when coevolution was possible: reduced antagonism evolved in the copassaged treatment. Reduced antagonism, however, did not evolve when hosts or parasites were independently selected without coevolution. In addition, we found strong local adaptation for reduced antagonism between replicate host/parasite lines in the copassaged treatment. Taken together, these results strongly suggest that coevolution was critical to the rapid evolution of reduced antagonism.     

Long‐term selection experiment produces breakdown of horizontal transmissibility in parasite with mixed transmission mode

Evolutionary transitions from parasitism toward beneficial or mutualistic associations may encompass a change from horizontal transmission to (strict) vertical transmission. Parasites with both vertical and horizontal transmission are amendable to study factors driving such transitions. In a long‐term experiment, microcosm populations of the protozoan Paramecium caudatum and its bacterial parasite Holospora undulata were exposed to three growth treatments, manipulating vertical transmission opportunities over ca. 800 host generations. In inoculation tests, horizontal transmission propagules produced by parasites from a “high‐growth” treatment, with elevated host division rates increasing levels of parasite vertical transmission, showed a near‐complete loss of infectivity. A similar reduction was observed for parasites from a treatment alternating between high growth and low growth (i.e., low levels of population turn‐over). Parasites from a low‐growth treatment had the highest infectivity on all host genotypes tested. Our results complement previous findings of reduced investment in horizontal transmission and increased vertical transmissibility of high‐growth parasites. We explain the loss of horizontal transmissibility by epidemiological feedbacks and resistance evolution, reducing the frequency of susceptible hosts in the population and thereby decreasing the selective advantage of horizontal transmission. This illustrates how environmental conditions may push parasites with a mixed transmission mode toward becoming vertically transmitted nonvirulent symbionts.     

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.     

Diversification of transmission modes and the evolution of mutualism

In order for mutualism to evolve, some force must align the interests of the two interacting partners. Vertical transmission can fill this role, but it is still unknown whether mutualism can be stable when vertically transmitted symbionts can evolve toward horizontal transmission. In this article, we investigate how symbionts' transmission mode and virulence should evolve, depending on the relationship between these two traits. We show that pathogens that reduce their host's fecundity can have more complex evolutionary dynamics than those that increase mortality. In some cases, runaway evolution of virulence can drive the host population extinct. In most cases, evolutionary branching results in the differentiation of avirulent, vertically transmitted symbionts from virulent, contagious pathogens. The population of symbionts then becomes polymorphic, and because the least virulent symbionts are the most frequent, the average virulence of symbionts is much lower than it would be in a monomorphic population. When the link between transmission and virulence results from correlated mutational changes and not from fixed constraints, vertically transmitted symbionts do not simply lose virulence; they evolve toward mutualism. We show that the force that stabilizes mutualism in such situations is the competition for transmission between symbionts.     

Individual patterns of habitat and nest-site use by hosts promote transgenerational transmission of avian brood parasitism status

Brood parasitic birds impose variable fitness costs upon their hosts by causing the partial or complete loss of the hosts' own brood. Growing evidence from multiple avian host-parasite taxa indicates that exposure of individual hosts to parasitism is not necessarily random and varies with habitat use, nest-site selection, age or other phenotypic attributes. For instance, nonrandom patterns of brood parasitism had similar evolutionary consequences to those of limited horizontal transmission of parasites and pathogens across space and time and altered the dynamics of both population productivity and co-evolutionary interactions of hosts and parasites. We report that brood parasitism status of hosts of brown-headed cowbirds Molothrus ater is also transmitted across generations in individually colour-banded female prothonotary warblers Protonotaria citrea. Warbler daughters were more likely to share their mothers' parasitism status when showing natal philopatry at the scale of habitat patch. Females never bred in their natal nestboxes but daughters of parasitized mothers had shorter natal dispersal distances than daughters of nonparasitized mothers. Daughters of parasitized mothers were more likely to use nestboxes that had been parasitized by cowbirds in both the previous and current years. Although difficult to document in avian systems, different propensities of vertical transmission of parasitism status within host lineages will have critical implications both for the evolution of parasite tolerance in hosts and, if found to be mediated by lineages of parasites themselves, for the difference in virulence between such extremes as the nestmate-tolerant and nestmate-eliminator strategies of different avian brood parasite species.     

Transmission and burden and the impact of temperature on two species of vertically transmitted microsporidia

Microsporidia are unusual amongst eukaryotic parasites in that they utilize both vertical and horizontal transmission and vertically transmitted species can cause sex ratio distortion in their host. Here we study vertical transmission in two species of feminising microsporidia, Nosema granulosis and Dictyocoela duebenum, infecting a single population of the crustacean host Gammarus duebeni and measure the effect of temperature on parasite transmission and replication. N. granulosis was vertically transmitted to 82% of the host embryos and D. duebenum was transmitted to 72% of host embryos. For both parasites, we report relatively low parasite burdens in developing host embryos. However, the parasites differ in their pattern of replication and burden within developing embryos. Whilst N. granulosis undergoes replication during host development, the burden of D. duebenum declines, leading us to propose that parasite dosage and feminisation efficiency underlie the different parasite frequencies in the field. We also examine the effect of temperature on parasite transmission and replication. Temperature does not affect the percentage of young that inherit the infection. However, low temperatures inhibit parasite replication relative to host cell division, resulting in a reduction in parasite burden in infected embryos. The reduced parasite burden at low temperatures may underpin reduced feminization at low temperatures and so limit the spread of sex ratio distorters through the host population.     

Ecological genomics of mutualism decline in nitrogen-fixing bacteria

Anthropogenic changes can influence mutualism evolution; however, the genomic regions underpinning mutualism that are most affected by environmental change are generally unknown, even in well-studied model mutualisms like the interaction between legumes and their nitrogen (N)-fixing rhizobia. Such genomic information can shed light on the agents and targets of selection maintaining cooperation in nature. We recently demonstrated that N-fertilization has caused an evolutionary decline in mutualistic partner quality in the rhizobia that form symbiosis with clover. Here, population genomic analyses of N-fertilized versus control rhizobium populations indicate that evolutionary differentiation at a key symbiosis gene region on the symbiotic plasmid (pSym) contributes to partner quality decline. Moreover, patterns of genetic variation at selected loci were consistent with recent positive selection within N-fertilized environments, suggesting that N-rich environments might select for less beneficial rhizobia. By studying the molecular population genomics of a natural bacterial population within a long-term ecological field experiment, we find that: (i) the N environment is indeed a potent selective force mediating mutualism evolution in this symbiosis, (ii) natural variation in rhizobium partner quality is mediated in part by key symbiosis genes on the symbiotic plasmid, and (iii) differentiation at selected genes occurred in the context of otherwise recombining genomes, resembling eukaryotic models of adaptation.     

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.     

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.     

Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence

Interactions involving several parasite species (multi-parasitized hosts) or several host species (multi-host parasites) are the rule in nature. Only a few studies have investigated these realistic, but complex, situations from an evolutionary perspective. Consequently, their impact on the evolution of parasite virulence and transmission remains poorly understood. The mechanisms by which multiple infections may influence virulence and transmission include the dynamics of intrahost competition, mediation by the host immune system and an increase in parasite genetic recombination. Theoretical investigations have yet to be conducted to determine which of these mechanisms are likely to be key factors in the evolution of virulence and transmission. In contrast, the relationship between multi-host parasites and parasite virulence and transmission has seen some theoretical investigation. The key factors in these models are the trade-off between virulence across different host species, variation in host species quality and patterns of transmission. The empirical studies on multi-host parasites suggest that interspecies transmission plays a central role in the evolution of virulence, but as yet no complete picture of the phenomena involved is available. Ultimately, determining how complex host–parasite interactions impact the evolution of host–parasite relationships will require the development of cross-disciplinary studies linking the ecology of quantitative networks with the evolution of virulence.     

Contact transmission of Tobacco mosaic virus: a quantitative analysis of parameters relevant for virus evolution

Transmission between hosts is required for the maintenance of parasites in the host population and determines their ultimate evolutionary success. The transmission ability of parasites conditions their evolution in two ways: on one side, it affects the genetic structure of founded populations in new hosts. On the other side, parasite traits that increase transmission efficiency will be selected for. Therefore, knowledge of the factors and parameters that determine transmission efficiency is critical to predict the evolution of parasites. For plant viruses, little is known about the parameters of contact transmission, a major way of transmission of important virus genera and species. Here, we analyze the factors determining the efficiency of contact transmission of Tobacco mosaic virus (TMV) that may affect virus evolution. As it has been reported for other modes of transmission, the rate of TMV transmission by contact depended on the contact opportunities between an infected and a noninfected host. However, TMV contact transmission differed from other modes of transmission, in that a positive correlation between the virus titer in the source leaf and the rate of transmission was not found within the range of our experimental conditions. Other factors associated with the nature of the source leaf, such as leaf age and the way in which it was infected, had an effect on the rate of transmission. Importantly, contact transmission resulted in severe bottlenecks, which did not depend on the host susceptibility to infection. Interestingly, the effective number of founders initiating the infection of a new host was highly similar to that reported for aphid-transmitted plant viruses, suggesting that this trait has evolved to an optimum value.     

HOST GROWTH CONDITIONS INFLUENCE EXPERIMENTAL EVOLUTION OF LIFE HISTORY AND VIRULENCE OF A PARASITE WITH VERTICAL AND HORIZONTAL TRANSMISSION

In parasites with mixed modes of transmission, ecological conditions may determine the relative importance of vertical and horizontal transmission for parasite fitness. This may lead to differential selection pressure on the efficiency of the two modes of transmission and on parasite virulence. In populations with high birth rates, increased opportunities for vertical transmission may select for higher vertical transmissibility and possibly lower virulence. We tested this idea in experimental populations of the protozoan Paramecium caudatum and its bacterial parasite Holospora undulata. Serial dilution produced constant host population growth and frequent vertical transmission. Consistent with predictions, evolved parasites from this “high‐growth” treatment had higher fidelity of vertical transmission and lower virulence than parasites from host populations constantly kept near their carrying capacity (“low‐growth treatment”). High‐growth parasites also produced fewer, but more infectious horizontal transmission stages, suggesting the compensation of trade‐offs between vertical and horizontal transmission components in this treatment. These results illustrate how environmentally driven changes in host demography can promote evolutionary divergence of parasite life history and transmission strategies.     

SELECTION OF BENEVOLENCE IN A HOST–PARASITE SYSTEM

A paradigm for the evolution of cooperation between parasites and their hosts argues that the mode of parasite transmission is critical to the long-term maintenance of cooperation. Cooperation is not expected to be maintained whenever the chief mode of transmission is horizontal: a parasite's progeny infect hosts unrelated to their parent's host. Cooperation is expected to be maintained if the chief mode of transmission is vertical: a parasite's progeny infect only the parent's host or descendants of that host. This paradigm was tested using bacteria and filamentous bacteriophage (f1). When cells harboring different variants of these phage were cultured so that no infectious spread was allowed, ensuring that all parasite transmission was vertical, selection favored the variants that were most benevolent to the host—those that least harmed host growth rate. By changing the culture conditions so that horizontal spread of the phage was allowed, the selective advantage of the benevolent forms was lost. These experiments thus support the theoretical arguments that mode of transmission is a major determinant in the evolution of cooperation between a parasite and its host.     

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.