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 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.     

Multiple Symbiont Acquisition Strategies as an Adaptive Mechanism in the Coral Stylophora pistillata

In obligate symbioses, the host’s survival relies on the successful acquisition and maintenance of symbionts. Symbionts can either be transferred from parent to offspring via direct inheritance (vertical transmission) or acquired anew each generation from the environment (horizontal transmission). With vertical symbiont transmission, progeny benefit by not having to search for their obligate symbionts, and, with symbiont inheritance, a mechanism exists for perpetuating advantageous symbionts. But, if the progeny encounter an environment that differs from that of their parent, they may be disadvantaged if the inherited symbionts prove suboptimal. Conversely, while in horizontal symbiont acquisition host survival hinges on an unpredictable symbiont source, an individual host may acquire genetically diverse symbionts well suited to any given environment. In horizontal acquisition, however, a potentially advantageous symbiont will not be transmitted to subsequent generations. Adaptation in obligate symbioses may require mechanisms for both novel symbiont acquisition and symbiont inheritance. Using denaturing-gradient gel electrophoresis and real-time PCR, we identified the dinoflagellate symbionts (genus Symbiodinium) hosted by the Red Sea coral Stylophora pistillata throughout its ontogenesis and over depth. We present evidence that S. pistillata juvenile colonies may utilize both vertical and horizontal symbiont acquisition strategies. By releasing progeny with maternally derived symbionts, that are also capable of subsequent horizontal symbiont acquisition, coral colonies may acquire physiologically advantageous novel symbionts that are then perpetuated via vertical transmission to subsequent generations. With symbiont inheritance, natural selection can act upon the symbiotic variability, providing a mechanism for coral adaptation.     

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.     

The evolutionary ecology of symbiont‐conferred resistance to parasitoids in aphids

Aphids may harbor a wide variety of facultative bacterial endosymbionts. These symbionts are transmitted maternally with high fidelity and they show horizontal transmission as well, albeit at rates too low to enable infectious spread. Such symbionts need to provide a net fitness benefit to their hosts to persist and spread. Several symbionts have achieved this by evolving the ability to protect their hosts against parasitoids. Reviewing empirical work and some models, I explore the evolutionary ecology of symbiont‐conferred resistance to parasitoids in order to understand how defensive symbiont frequencies are maintained at the intermediate levels observed in aphid populations. I further show that defensive symbionts alter the reciprocal selection between aphids and parasitoids by augmenting the heritable variation for resistance, by increasing the genetic specificity of the host–parasitoid interaction, and by inducing environment‐dependent trade‐offs. These effects are conducive to very dynamic, symbiont‐mediated coevolution that is driven by frequency‐dependent selection. Finally I argue that defensive symbionts represent a problem for biological control of pest aphids, and I propose to mitigate this problem by exploiting the parasitoids’ demonstrated ability to rapidly evolve counteradaptations to symbiont‐conferred resistance.     

Population genetics of beneficial heritable symbionts

Most species of insects are infected with heritable, facultative symbionts. Such symbionts first appear within a host lineage as a result of lateral transfer from other host species. Although some facultative symbionts are reproductive parasites and thus adversely affect the transmission of host nuclear genes, there is growing evidence that many are beneficial to their hosts by, for example, conferring protection from natural enemies. The origin, spread, and maintenance of such symbionts bears many similarities to, as well as important differences from, the process of adaptive evolution by beneficial nuclear mutations. The time is ripe for the development of a coherent theory of the 'population genetics' of beneficial heritable symbionts.     

Co-niche construction between hosts and symbionts: ideas and evidence

Symbiosis is a process that can generate evolutionary novelties and can extend the phenotypic niche space of organisms. Symbionts can act together with their hosts to co-construct host organs, within which symbionts are housed. Once established within hosts, symbionts can also influence various aspects of host phenotype, such as resource acquisition, protection from predation by acquisition of toxicity, as well as behaviour. Once symbiosis is established, its fidelity between generations must be ensured. Hosts evolve various mechanisms to screen unwanted symbionts and to facilitate faithful transmission of mutualistic partners between generations. Microbes are the most important symbionts that have influenced plant and animal phenotypes; multicellular organisms engage in developmental symbioses with microbes at many stages in ontogeny. The co-construction of niches may result in composite organisms that are physically nested within each other. While it has been advocated that these composite organisms need new evolutionary theories and perspectives to describe their properties and evolutionary trajectories, it appears that standard evolutionary theories are adequate to explore selection pressures on their composite or individual traits. Recent advances in our understanding of composite organisms open up many important questions regarding the stability and transmission of these units.     

Can interspecies affairs in the dark lead to evolutionary innovation?

Evolutionary adaptation is the adjustment of species to a new or changing environment. Engaging in mutualistic microbial symbioses has been put forward as a key trait that promotes the differential, evolutionary success of many animal and plant lineages (McFall‐Ngai, 2008). Microbial mutualists allow these organisms to occupy new ecological niches where they could not have persisted on their own or would have been constrained by competitors. Vertical transmission of beneficial microbial symbionts from parents to the offspring is expected to link the adaptive association between a given host and microbe, and it can lead to coevolution and sometimes even cospeciation (Fisher, Henry, Cornwallis, Kiers, & West, 2017). Vertical transmission also causes bottlenecks that strongly reduce the effective population size and genetic diversity of the symbiont population. Moreover, vertically transmitted symbionts are assumed to have fewer opportunities to exchange genes with relatives in the environment. In a “From the Cover” article in this issue of Molecular Ecology, Breusing, Johnson, Vrijenhoek, and Young (2019) investigated whether hybridization among different host species could lead to interspecies exchange of otherwise strictly vertically transmitted symbionts. Hybridization of divergent lineages can potentially cause intrinsic and extrinsic incompatibilities, swamp rare alleles, and lead to population extinctions. In some cases, however, it might also create novel trait combinations that lead to evolutionary innovation (Marques, Meier, & Seehausen, 2019). Breusing et al. (2019) linked the concept of hybridization to symbiont transmission, and their findings have significant implications for the study of evolution of vertically transmitted symbionts and their hosts.     

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.     

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.     

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.     

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.     

A slowly evolving host moves first in symbiotic interactions

Symbiotic relationships, both parasitic and mutualistic, are ubiquitous in nature. Understanding how these symbioses evolve, from bacteria and their phages to humans and our gut microflora, is crucial in understanding how life operates. Often, symbioses consist of a slowly evolving host species with each host only interacting with its own subpopulation of symbionts. The Red Queen hypothesis describes coevolutionary relationships as constant arms races with each species rushing to evolve an advantage over the other, suggesting that faster evolution is favored. Here, we use a simple game theoretic model of host-symbiont coevolution that includes population structure to show that if the symbionts evolve much faster than the host, the equilibrium distribution is the same as it would be if it were a sequential game where the host moves first against its symbionts. For the slowly evolving host, this will prove to be advantageous in mutualisms and a handicap in antagonisms. The result follows from rapid symbiont adaptation to its host and is robust to changes in the parameters, even generalizing to continuous and multiplayer games. Our findings provide insight into a wide range of symbiotic phenomena and help to unify the field of coevolutionary theory.     

Intracellular symbionts and the evolution of uniparental cytoplasmic inheritance.

Uniparental inheritance of cytoplasmic elements is widespread among eukaryotic organisms and is achieved by a diverse range of mechanisms. This paper shows that the cytoplasmic genetic system would be expected to evolve towards uniparental inheritance, given the existence of deleterious symbionts capable of invading the host cytoplasm together with nuclear genes that lead to the elimination of cytoplasmic elements from one of the gamete types. The reason for this is that, under biparental inheritance, foreign symbionts with strong deleterious effects are able to spread through host populations. A nuclear modifier gene which leads to the loss of cytoplasmic elements from one gamete type gains a net advantage as a symbiont spreads, because the modifier sometimes gives rise to a symbiont-free zygote. Insofar as small gametes reduce the rate of symbiont transmission to the zygote, modifier genes causing small gamete size would tend to accumulate, so that cytoplasmic inheritance would become associated with maternal rather than paternal gametes. Once uniparental inheritance predominates in the host population, the population is protected from invasions by a large class of harmful symbionts, but at the same time those symbionts that benefit their hosts are still able to increase in frequency.     

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.     

Symbiont-mediated protection

Despite the fact that all vertically transmitted symbionts sequester resources from their hosts and are therefore costly to maintain, there is an extraordinary diversity of them in invertebrates. Some spread through host populations by providing their hosts with fitness benefits or by manipulating host sex ratio, but some do not: their maintenance in host lineages remains an enigma. In this review, I explore the evolutionary ecology of vertically transmitted symbionts and their impact on host resistance, and provide an overview of the evidence for the three-way interactions between these symbionts, natural enemies and invertebrate hosts. A number of recent empirical and theoretical studies suggest that vertically transmitted symbionts may protect their hosts from pathogens. If this 'symbiont-mediated protection' is widespread, it is likely that vertically transmitted symbionts contribute significantly to variation in measures of invertebrate resistance to natural enemies.     

Vertical transmission as the key to the colonization of Madagascar by fungus-growing termites?

The mutualism between fungus-growing termites (Macrotermitinae) and their mutualistic fungi (Termitomyces) began in Africa. The fungus-growing termites have secondarily colonized Madagascar and only a subset of the genera found in Africa is found on this isolated island. Successful long-distance colonization may have been severely constrained by the obligate interaction of the termites with fungal symbionts and the need to acquire these symbionts secondarily from the environment for most species (horizontal symbiont transmission). Consistent with this hypothesis, we show that all extant species of fungus-growing termites of Madagascar are the result of a single colonization event of termites belonging to one of the only two groups with vertical symbiont transmission, and we date this event at approximately 13 Mya (Middle/Upper Miocene). Vertical symbiont transmission may therefore have facilitated long-distance dispersal since both partners disperse together. In contrast to their termite hosts, the fungal symbionts have colonized Madagascar multiple times, suggesting that the presence of fungus-growing termites may have facilitated secondary colonizations of the symbiont. Our findings indicate that the absence of the right symbionts in a new environment can prevent long-distance dispersal of symbioses relying on horizontal symbiont acquisition.     

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.