Abstract
Symbiosis can benefit hosts in numerous ways, but less is known about whether interactions with hosts benefit symbionts—the smaller species in the relationship. To determine the fitness impact of host association on symbionts in likely mutualisms, we conducted a meta-analysis across 91 unique host-symbiont pairings under a range of spatial and temporal contexts. Specifically, we assess the consequences to symbiont fitness when in and out of symbiosis, as well as when the symbiosis is under suboptimal or varying environments and biological conditions (e.g., host age). We find that some intracellular symbionts associated with protists tend to have greater fitness when the symbiosis is under stressful conditions. Symbionts of plants and animals did not exhibit this trend, suggesting that symbionts of multicellular hosts are more robust to perturbations. Symbiont fitness also generally increased with host age. Lastly, we show that symbionts able to proliferate in- and outside host cells exhibit greater fitness than those found exclusively inside or outside cells. The ability to grow in multiple locations may thus help symbionts thrive. We discuss these fitness patterns in light of host-driven factors, whereby hosts exert influence over symbionts to suit their own needs.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
1 Introduction
Long-term associations with symbionts, or symbioses, have had a major influence on the evolution of life on Earth (Margulis and Fester 1991). In beneficial symbioses, symbionts provide hosts with nutrients they would not otherwise be able to utilize (Douglas 1998), with protection from harsh conditions or enemies (Latef et al. 2016; Corbin et al. 2017; King 2019), or with general development and maturation (McFall-Ngai 2002). By contrast, the symbiont is often assumed to benefit from the association, such as provisioning of nutrients and stable environments by the host (Wollenberg and Ruby 2012; Feng et al. 2019)), but recent evidence suggests that associations previously assumed to be mutualistic are not actually beneficial for symbionts (McCutcheon et al. 2019).
From an evolutionary perspective, a mutualism occurs when both partners exhibit a net fitness increase when in symbiosis compared to when free-living. However, symbioses are often context-dependent. Hosts might only benefit under certain ecological contexts (Drew et al. 2021). Similarly, variation in symbiont fitness can be attributed to multiple factors: host biology, symbiont biology, the environment, or some combination thereof (Dossi et al. 2014; López-Madrigal and Duarte 2020). Benefits provided to the symbiont might depend on whether the symbiosis occurs under optimal conditions. For example, hosts may support symbiont growth only when the symbiosis is under perturbation. These conditions include lack of resources, presence of enemies, and co-colonization of multiple symbiont strains, all of which can be stressful for the host (Scarborough et al. 2005; Lau et al. 2012; Oliver et al. 2013; Weldon et al. 2019). In addition to environmental factors, symbiont fitness can also vary over time, including on the scale of a host generation. Symbionts may accumulate across the duration of the symbiosis, or gain more space to grow as hosts develop (Wollenberg and Ruby 2009; Kikuchi et al. 2011). Despite the critical roles symbionts can have in host health and adaptation, it is generally unclear whether symbiosis confers a fitness advantage to symbionts (Douglas and Smith 1989; Garcia and Gerardo 2014).
Here, we test the assumption that symbionts exhibit fitness gains in beneficial symbioses and are robust to perturbation. We examine the effects of environmental and temporal contexts on symbiont fitness in associations where the symbiont provides benefits to the host in at least some contexts. Specifically, our main hypotheses are that symbiont fitness is greater (Hypothesis 1) when in symbiosis as opposed to in a free-living state, and (Hypothesis 2) when the symbiosis is under non-stressful conditions. Alternatively, symbiont fitness could be greater when the symbiosis is under non-optimal conditions. Our third main hypothesis (Hypothesis 3) is that greater symbiont fitness is more common in older hosts. Across time, greater within-host symbiont density is expected as the host has more resources to support symbiont growth (Feng et al. 2019; Fronk and Sachs 2022). An increase in host size over time would also provide more space for symbiont growth (e.g., (Kerwin et al. 2021)).
To test these hypotheses, we conducted a literature search for studies measuring symbiont fitness to evaluate whether and how fitness varies in different environments and throughout host development. We collected data on aspects of host biology, including kingdom (Bermudes and Margulis 1987), reproductive mode (Law and Lewis 1983), and generation time (Takahashi 2016), which may play roles in moderating symbiont fitness. We also collected information on symbiont traits, including symbiont diversity (Foster et al. 2017), location of symbiont on/in hosts (Chomicki et al. 2020), and genome size (Fisher et al. 2017), in addition to the type of association and level of dependence on the host (Fisher et al. 2017), to determine whether symbiont fitness varies for these categories. These variables are summarized in Table 1.
2 Materials and methods
2.1 Literature search and data collection
To evaluate symbiont fitness across different contexts, we conducted a literature search on ISI Web of Science. We used a combination of search terms relating to symbiont fitness, host factors, and host-microbe interactions (specific terms are found in Figure S1). We then identified additional studies by looking through the references of relevant papers and the studies that cited these papers. We included papers that met the following criteria in our analyses:
-
1.
The study measured symbiont fitness in different environments (either outside/without host or under varying abiotic/biotic conditions, such as temperature, resources, or presence of other species) or the study measured symbiont fitness under at least two different time points across the lifespan of the host.
-
2.
The symbiont being examined was considered a beneficial symbiont (e.g., providing the host with tangible or fitness benefits under some context). If its function was unknown, it was at least commonly found in the host population and did not show signs of parasitism.
-
3.
The symbiont was classified at least at the family level as broader classifications did not allow for more specific information to be discerned about the symbiont.
-
4.
Information existed for the variance of each fitness mean estimate.
A plot of all effect sizes from eligible studies, including those removed from the analyses (i.e., those meeting all but the last criterion), is shown in Figure S2.
The search resulted in 63 studies (161 effect sizes) that matched our inclusion criteria from studies published between 1994 (the earliest study meeting our criteria) and 2020 (when we started the literature search). For each study, we extracted data using WebDigiPlot (Rohatgi 2021), or contacted authors if relevant information or raw data were not available. We then parsed out the results according to the conditions under which fitness was measured: 11 studies (20 effect sizes) were used in the host association analysis, 50 studies (119 effect sizes) were used in the environment analysis, and 25 studies (42 effect sizes) were used in the time analysis. We also created a subset of the environmental dataset to include only intracellular symbionts (17 studies, 47 effect sizes) to examine how symbiont fitness changes when confined inside host cells. While the majority of the symbionts in our analysis are microbial (e.g., bacteria and fungi), we also included animal symbionts. In such cases, the symbiont is the species that has multiple individuals in symbiosis with one host individual. For example, in the crayfish-branchiobdellidan worm cleaning symbiosis (Thomas et al. 2013), the worm is the symbiont because multiple worms inhabit one crayfish individual. We identified 47 host species and 78 symbiont species from our search, resulting in 91 unique host-symbiont pairings. Host and symbiont phylogenies are included in the meta-analyses (Fig. 1, Table S1), while the types of host and symbiont are in Figures S3A and S3B, respectively.
2.2 Effect size calculation
To test Hypothesis 1 (whether symbiont fitness is greater outside of symbiosis), we collected fitness measurements for symbionts from studies where symbionts are inside or on the surface of the host vs. when they are outside of the host (where the host may still be present); or from studies where the host is present vs. absent. While the two contexts (inside vs. outside and presence vs. absence of host) may provide different insights into the role of the host on symbiont fitness (e.g., presence vs. absence of host control for the environment and volume in which symbionts grow), there are not enough studies for either context to be analyzed separately. We then calculated the percent change in symbiont fitness (the effect size) using the formula:
To test Hypothesis 2 (whether fitness is greater when the symbiosis is under stress), we collected fitness measurements for the symbiont in a control environment and in an alternative environment. We designated a treatment as the “control” environment when the symbiont interacted with its host at ambient conditions in the absence of other organisms (i.e., those present in the alternative environment); this is representative of the “focal” symbiosis between host and symbiont. The alternative environment indicates one where the symbiosis is experiencing suboptimal or stressful conditions, having negative impacts on host or symbiont performance or fitness (Schulte 2014), or may affect the stability of the interaction (e.g., causing one partner to be lost), relative to the control condition. We used the formula:
To test Hypothesis 3, in that symbiont fitness decreases as hosts age, we considered the “control” treatment to be when the host is younger, using the formula:
Our study included a diverse range of fitness measures, including area of host colonized, colony forming units (CFU), count, density, fluorescence, growth rate, nodule number, sequences and survival. To compare effect sizes, we converted the difference in fitness means between the control and experimental treatments from each study into a percentage for our analyses (similar to (Fisher et al. 2017)) to standardize across the different fitness measurements (Figure S3C), which vary in scale across systems (e.g., nodule number vs. number of colony forming units). To calculate the variance of the percent change, we used the formula from Appendix 6 of Haney et al. (2007). Lastly, we cube-root transformed (to preserve positive and negative values) the final percent change and variance values due to the presence of several very large effect sizes.
2.3 Symbiont and host phylogeny construction
Phylogenetic relatedness can be a source of non-independence between effect sizes—closely related symbionts may respond in the same way to selective pressures, or closely related hosts can similarly affect symbionts (Murfin et al. 2015). To account for phylogenetic non-independence in our models, we constructed phylogenies of the symbionts and hosts included in our analyses. We pruned the tree available at the Open Tree of Life (OTL) with the R packages rotl and ape to build trees containing our species of interest and visualized them using the phytools package (Revell 2012; Michonneau et al. 2016; Paradis and Schliep 2019). When a species was not found in OTL, we found the closest relative available in the genus or family (10 instances; Table S2), then substituted it in place of the missing species. Because some species have more than one effect size, we generated trees such that each species was classified at the population level to match with their corresponding effect size. The phylogenetic distances between “populations” of the same species were < < 0.00001 (effectively zero), but the population-level designation allow us to distinguish between populations from different studies. We then converted the phylogenies into correlation matrices assuming Brownian motion to incorporate into our phylogenetically-informed meta-analyses.
2.4 Statistical analysis
We conducted separate analyses for the host association, environment, and time datasets using the R package metafor (Viechtbauer 2010). We built multi-level mixed-effects models using the rma.mv function restricted maximum likelihood estimation of parameters. To account for some studies having multiple effect sizes, we included between-study effects and within-study effects as random factors (Noble et al. 2017). We ran the models treating symbiont phylogeny as a random effect, then re-ran the models treating host phylogeny as a random effect. Because results were qualitatively the same for both phylogenies, we present the results for incorporation of symbiont phylogeny. We then conducted moderator analyses using a Wald-type test (QM statistic) to examine the effects of specific variables on symbiont fitness (Table 1) (Viechtbauer 2010). For the environment dataset, we also examined a subset of effect sizes that belonged to intracellular symbionts and included host generation time as a moderator variable. For hosts associated with multiple symbionts (or vice versa), we ran the analysis for each unique host-symbiont pairing or for each unique symbiont. For symbionts with multiple effect sizes, we used the mean effect size. To identify potential outliers, we calculated Cook’s distance (D) for each analysis and removed effect sizes that had D greater than three times the mean (Cook 1977). All statistical analyses were conducted in R (R Core Team 2021).
3 Results
3.1 Host association has no significant effects on symbiont fitness
The results did not support our first hypothesis: there was no significant effect of host association on symbiont fitness (z = -0.627, p = 0.531; Fig. 2A). Neither the direction or magnitude of the effect size was influenced by host kingdom (QM = 0.755, df = 2, p = 0.686; Fig. 2B), symbiont diversity (QM = 0.027, df = 1, p = 0.871; Fig. 2C), host reproductive mode (QM = 0.046, df = 1, p = 0.831; Fig. 2D), symbiont location (QM = 0.046, df = 1, p = 0.831; Fig. 2E), or genome size (QM = 0.407, df = 1, p = 0.524). The type of association and symbiont dependence on host were marginally significant (QM = 6.809, df = 3, p = 0.078 and QM = 3.211, df = 1, p = 0.073, respectively; Figs. 2F and 2G). Table S3 contains the results for all overall and moderator analyses, with all effect sizes or with outliers removed.
3.2 Animal-associated symbionts have opposing trends to protist-associated symbionts
There was no significant overall effect of environment on symbiont fitness (Hypothesis 2, z = -0.509, p = 0.611; Fig. 3A). The direction and magnitude of the effect size were not influenced by host kingdom (QM = 2.899, df = 2, p = 0.235; Fig. 3B), type of association (QM = 2.124, df = 3, p = 0.547; Fig. 3C), symbiont dependence on host (QM = 0.025, df = 1, p = 0.874; Fig. 3D), symbiont diversity (QM = 0.358, df = 2, p = 0.836; Fig. 3E), host reproductive mode (QM = 0.985, df = 1, p = 0.321; Fig. 3F), location of symbiont (QM = 0.402, df = 2, p = 0.818; Fig. 3G), or genome size (QM = 0.641, df = 1, p = 0.423). However, when outliers were removed, host kingdom was significant (QM = 7.300, df = 2, p = 0.026), particularly for intracellular symbionts (QM = 12.25, df = 2, p = 0.002; Fig. 4A). Protists harbored symbionts that performed better when in suboptimal environments. Symbiont fitness may be tied to host cell division for intracellular symbionts. For example, unicellular hosts and their symbionts undergo synchronized cell division (Kadono et al. 2004; Motta et al. 2010), where a shorter host generation time may prevent symbionts from accumulating. We therefore examined whether host generation time was correlated with change in symbiont fitness and found no correlation when accounting for each unique host-symbiont pairing (QM = 2.191, p = 0.139; Fig. 4B). However, when accounting for each unique symbiont (regardless of the host associated with the symbiont), symbiont fitness was positively correlated with host generation time (QM = 5.036, p = 0.025; Fig. 4C) and symbiont genome size (QM = 4.524, p = 0.033; Fig. 4D).
3.3 Symbiont fitness is greater in older hosts
To test Hypothesis 3, we examined how symbiont fitness changes over time. As hosts develop and increase in size, symbionts may acquire more space to grow or more time to proliferate (Wollenberg and Ruby 2009; Kikuchi et al. 2011). Our results supported this hypothesis: there was a significant effect of time on the percent change in symbiont fitness, where fitness increased overall in older hosts (z = -2.524, p = 0.012; Fig. 5A). However, there were some studies in which symbiont fitness increased to a certain point, then subsequently declined (Rio et al. 2006; Hamidou Soumana et al. 2013; Vigneron et al. 2014; Zhao et al. 2018; Garcia et al. 2019). Since our criterion was to record symbiont fitness at the timepoint when hosts were the oldest in each study, the effect sizes from the above studies could have been greater if peak fitness had been recorded instead. Host life stage was a significant moderator variable (QM = 6.235; df = 2, p = 0.044; Fig. 5B), with symbiont fitness tend to be greater in adults when compared to the juvenile stage. Conversely, host kingdom (QM = 3.539, df = 2, p = 0.170; Fig. 5C), type of association (QM = 0.235, df = 3, p = 0.972; Fig. 5D), symbiont dependence on host (QM = 0.213, df = 1, p = 0.645; Fig. 5E), symbiont diversity (QM = 2.467, df = 2, p = 0.291; Fig. 5F), host reproductive mode (QM = 3.569, df = 3, p = 0.312; Fig. 5G), and symbiont genome size (QM = 0.006, df = 1, p = 0.940) did not influence the direction or magnitude of the effect size.
Symbionts able to grow outside host cells (which include the space between cells within a host or on host surfaces) should perform better than those confined to host cells. This hypothesis was partially supported: symbionts found both inside and outside cells tended to have greater fitness when hosts were older, whereas such pattern was not found for exclusively intracellular or extracellular symbionts (QM = 8.609, df = 2, p = 0.014; Fig. 5H). Similar to the host association and environmental analyses, there was high variation in terms of symbiont fitness across studies and systems.
3.4 Outlier sensitivity analysis
Removal of outliers did not change the mean significance level for all but two of our results (Table S3), where the host kingdom moderator influenced symbiont fitness in different environments, and this effect was greater in intracellular symbionts.
4 Discussion
Overall, we did not find support for the hypothesis that symbionts gain a fitness benefit when host-associated. This finding could be due to ongoing conflicts between hosts and symbionts. Indeed, mutualism has been viewed as exploitation between partners that result in a net fitness benefit for both (Herre et al. 1999). Exploitation by symbionts is predicted due to their rapid evolution, similarities to pathogens, and the context-dependency under which benefits are provided to hosts (Davitt et al. 2011; Sachs et al. 2011; Weldon et al. 2013). Conversely, research has also indicated that hosts can take advantage of their symbionts before reciprocating benefits (Sorensen et al. 2019). Hosts can modify the growth of their symbionts in a variety of ways (Box 1)—from farming (Currie 2001), to compartmentalization (Chomicki et al. 2020), to expulsion (Thomas et al. 2013), to active culling (Vigneron et al. 2014; Piquet et al. 2019), increasing or decreasing symbiont abundance to suit host interests. Consequently, such regulation of symbiont population size may have resulted in no net fitness gain or loss across studies included in our analyses.
Symbionts not gaining from being in symbiosis may also be partly attributed to how fitness is quantified across studies. Measuring symbiont fitness inside versus outside the host is one way in which benefits are evaluated, but the space occupied by the symbiont is vastly different in the host and external environment (Douglas and Smith 1989). For example, there is less space for growth inside the host. Comparisons would have to be made in an environment of comparable volume to the host while also taking into consideration symbiont density in these spaces. The tested environment may also not be representative of the conditions in which symbionts are found in nature (e.g., rich media). Recent efforts have developed methods to compare symbiont populations in environments where the host is either present or absent (Burghardt et al. 2018; Burghardt 2019; Garcia et al. 2019; Mendoza-Suárez et al. 2020). With this approach, the volume of space is the same across all measurements and both partners occupy the same type of environment. However, there is a lack of studies measuring symbiont fitness inside vs. outside the host and in the presence vs. absence of hosts in general.
Our literature search yielded few studies where symbiont fitness was measured in and out of symbiosis, regardless of whether they were outside of the host or growing in the absence of the host. The lack of these studies could be representative of the proportion of symbionts able to thrive without host help. Because these symbioses lacked quantitative information on symbiont fitness, we were unable to include them. Well-known examples of these associations from the literature (e.g., (Fisher et al. 2017)) are presented in Figure S6, consisting of 60 unique host species and 35 unique symbiont species. Conversely, the lack of studies may be due to less emphasis on symbiont traits in the literature. There is a need for more experiments investigating the role of host association on symbiont fitness in general.
4.1 Symbiont fitness across environments
We found that single-celled hosts tend to harbor symbionts that incur costs under benign conditions compared to when stressed. The difference in symbiont abundance could be due to attributes of single-celled and multicellular hosts themselves. For example, unicellular eukaryotes (i.e., protists) are considered extant models for when symbioses first evolved (Gavelis and Gile 2018). As such, unicellular hosts may lack the ability to regulate their symbiont populations, thus more symbionts are free to grow when conditions are unstable. Conversely, animal and plant hosts potentially have had a longer evolutionary history with their symbionts and have evolved more robust methods of regulation (e.g., facilitation through nutrient provisioning (Feng et al. 2019) and specialized cells for housing symbionts (McFall-Ngai 2008; Chomicki et al. 2020)). These mechanisms allow for high symbiont population sizes when conditions are optimal, and low population sizes when conditions are stressful.
We also found that longer host generation time is correlated with higher intracellular symbiont fitness when under optimal conditions. Protists generally have shorter generation times than animals and plants. As host age is an important factor in symbiont fitness, the rapid turnover rates and shorter lifespan of protist hosts compared to animal hosts may not allow sufficient time for symbionts to accumulate in vivo. Alternatively, symbiont growth may not be host-driven. Symbionts may limit their own cell division within hosts when both partners benefit (Uchiumi et al. 2019). Having a larger genome tended to benefit symbionts in optimal conditions, which could also serve to reduce their dependence on the host for growth (Fisher et al. 2017). Regardless of the underlying mechanism, protist-microbe symbioses appear to support the stress gradient hypothesis. This hypothesis predicts that positive interactions between the partners will increase as conditions become more stressful (Bertness and Callaway 1994; Maestre et al. 2009; O’brien et al. 2018; Adams et al. 2022), where high levels of stress favors increased benefits for both partners. These findings may however be due to study limitations; single-celled hosts are more amenable to experiments and are model systems used in most studies of host exploitation (e.g., Lowe et al. 2016; Sorensen et al. 2019)).
4.2 Symbiont fitness across time
Several studies in our analysis saw symbiont fitness at a maximum before declining (Rio et al. 2006; Hamidou Soumana et al. 2013; Vigneron et al. 2014; Zhao et al. 2018; Garcia et al. 2019). It is possible that the hosts in these studies can regulate symbiont populations. One such mechanism is through the immune system, which is dynamic with host age. As hosts mature, the immune system may become more developed and robust to proliferating microbes (i.e., symbionts and pathogens) (Davidson et al. 2004; Johnston and Rolff 2015). Indeed, the largest differences in symbiont fitness were found between juvenile and adult life stages in our meta-analysis, with adults typically harboring more. As hosts age and may no longer require the symbiont, reducing symbiont population size could decrease costs associated with high symbiont titers (Vigneron et al. 2014; Chong and Moran 2016). Furthermore, symbionts found inside and outside host cells increased in abundance in older hosts—the ability to proliferate in multiple locations may allow symbionts to escape host regulation mechanisms. However, the same immune system is weakened as hosts senesce. This process may allow for accumulation of symbionts toward a level that is detrimental for hosts (Portal-Celhay et al. 2012). Identifying further links between host immunity, ageing, and microbial growth would advance understanding of temporal dynamics of symbiont density and the impact on host health.
4.3 Challenges in assessing symbiont fitness
Many effect sizes were on the order of magnitudes greater than the mean. The high variation across studies may be due to conceptual challenges of ascertaining symbiont fitness. Whether the symbiont benefits may depend on the context under which the symbiosis is scrutinized. At the molecular or physiological scale, provisions of host metabolites might suffice as a beneficial mechanism without a need for fitness measurements. However, from an ecological or evolutionary standpoint, increased fitness in symbiosis versus outside of symbiosis may be a better indicator of a reciprocal mutualism (Law and Dieckmann 1998; Mushegian and Ebert 2015). A classical test of mutualism calls for measuring fitness of one partner in the absence of the other (Douglas and Smith 1989; Wooldridge 2010; Mushegian and Ebert 2015), but this is likely not possible for symbionts that cannot be grown without hosts. Furthermore, any benefits identified from being in symbiosis for these symbionts may be confounded by their dependence on the host, and dependence may not actually require the exchange of benefits (Douglas and Smith 1989; Douglas 2015).
Whether the symbiont benefits from host association becomes even more complicated once a microbial community is involved. Symbiont fitness may not solely depend on the host but also other microbes present (Chamberlain et al. 2014; Mushegian and Ebert 2015; Song et al. 2020). Microbes can act as in vivo competitors or facilitators in a community context, further complicating the assessment of the fitness of any one particular symbiont. Moreover, symbiont persistence in host populations may not rely on total abundance in any individual host as much as transmission between hosts, whether from parent to offspring or dispersal to new environments (Lee and Ruby 1994; Brock et al. 2011; Ebert 2013; Thutupalli et al. 2017). Finally, the same fitness proxy cannot be applied across all symbiont types (e.g., percent of host cells occupied by the symbiont vs. nodule count), as with most multicellular hosts (e.g., survival or fecundity (Fisher et al. 2017)). Taken together, these perspectives suggest that there may not be a consensus as to how fitness should be evaluated for all symbionts.
5 Conclusion
Mutualistic symbiosis is often thought to involve reciprocal benefits. However, the mechanism underlying the interaction can be antagonistic—symbionts may not be free to proliferate while host-associated. Mechanisms of host regulation remain to be explored in many systems. Determining whether a symbiont is gaining from the association may require a combination of approaches to tackle. Extending research to additional and less-studied taxa will inform a better understanding of forces shaping symbiont fitness in general. Lastly, focusing on symbionts in and out of relationships with their multicellular hosts will lend further insight into the processes governing symbiont growth, such as elements of the host that change during senescence.
Data accessibility
Data used for analyses is publicly available in Mendeley Data: https://doi.org/10.17632/4rj49vkgtd.1.
References
Adams AE, Besozzi EM, Shahrokhi G, Patten MA (2022) A case for associational resistance: Apparent support for the stress gradient hypothesis varies with study system. Ecol Lett 25:202–217. https://doi.org/10.1111/ele.13917
Ankrah NYD, Chouaia B, Douglas E (2018) The cost of metabolic interactions in symbioses between insects and bacteria with reduced genomes. Mbio 9:1–15
Baghdasarian G, Muscatine L (2000) Preferential expulsion of dividing algal cells as a mechanism for regulating algal-cnidarian symbiosis. Biol Bull 199:278–286. https://doi.org/10.2307/1543184
Bermudes D, Margulis L (1987) Symbiont acquisition as neoseme: origin of species and higher taxa. Symbiosis 4:185–198
Bernhard JM, Bowser SS (1999) Benthic foraminifera of dysoxic sediments: Chloroplast sequestration and functional morphology. Earth Sci Rev 46:149–165. https://doi.org/10.1016/S0012-8252(99)00017-3
Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193. https://doi.org/10.1201/9780203738559
Brock DA, Douglas TE, Queller DC, Strassmann JE (2011) Primitive agriculture in a social amoeba. Nature 469:393–396. https://doi.org/10.1038/nature09668
Burghardt LT (2019) Evolving together, evolving apart: measuring the fitness of rhizobial bacteria in and out of symbiosis with leguminous plants. New Phytol. https://doi.org/10.1111/nph.16045
Burghardt LT, Epstein B, Guhlin J et al (2018) Select and resequence reveals relative fitness of bacteria in symbiotic and free-living environments. Proc Natl Acad 115:2425–2430. https://doi.org/10.1073/pnas.1714246115
Chamberlain SA, Bronstein JL, Rudgers JA (2014) How context dependent are species interactions? Ecol Lett 17:881–890. https://doi.org/10.1111/ele.12279
Chomicki G, Werner GDA, West SA, Kiers ET (2020) Compartmentalization drives the evolution of symbiotic cooperation. Philos Trans R Soc B Biol Sci 375. https://doi.org/10.1098/rstb.2019.0602rstb20190602
Chong RA, Moran NA (2016) Intraspecific genetic variation in hosts affects regulation of obligate heritable symbionts. Proc Natl Acad Sci USA 113:13114–13119. https://doi.org/10.1073/pnas.1610749113
Cook RD (1977) Detection of Influential Observation in Linear Regression. Technometrics 19:15–18. https://doi.org/10.1080/00401706.1977.10489493
Corbin C, Heyworth ER, Ferrari J, Hurst GDD (2017) Heritable symbionts in a world of varying temperature. Heredity (edinb) 118:10–20. https://doi.org/10.1038/hdy.2016.71
Currie CR (2001) A community of ants, fungi, and bacteria: a multilateral approach to studying symbiosis. Annu Rev Microbiol 55:357–380. https://doi.org/10.1146/annurev.micro.55.1.357
Davidson SK, Koropatnick TA, Kossmehl R et al (2004) NO means “yes” in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 6:1139–1151. https://doi.org/10.1111/j.1462-5822.2004.00429.x
Davitt AJ, Chen C, Rudgers JA (2011) Understanding context-dependency in plant-microbe symbiosis: the influence of abiotic and biotic contexts on host fitness and the rate of symbiont transmission. Environ Exp Bot 71:137–145. https://doi.org/10.1016/j.envexpbot.2010.11.004
Dossi FCA, da Silva EP, Cônsoli FL (2014) Population Dynamics and Growth Rates of Endosymbionts During Diaphorina citri (Hemiptera, Liviidae) Ontogeny. Microb Ecol 68:881–889. https://doi.org/10.1007/s00248-014-0463-9
Douglas AE (2015) The special case of symbioses: mutualisms with persistent contact. In: Bronstein JL (ed) Mutualism. Oxford University Press. https://doi.org/10.1093/acprof:oso/9780199675654.003.0002%0A
Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37. https://doi.org/10.1146/annurev.ento.43.1.17
Douglas AE, Smith DC (1989) Are endosymbioses mutualistic? Trends Ecol Evol 4:350–352
Drew GC, King KC (2022) More or less? The effect of symbiont density in defensive mutualisms. Am Nat 199:443–454. https://doi.org/10.1086/718593
Drew GC, Stevens EJ, King KC (2021) Microbial evolution and transitions along the parasite-mutualist continuum. Nat Rev Microbiol 19:623–638. https://doi.org/10.1038/s41579-021-00550-7
Ebert D (2013) The epidemiology and evolution of symbionts with mixed-mode transmission. Annu Rev Ecol Evol Syst 44:623–643. https://doi.org/10.1146/annurev-ecolsys-032513-100555
Feng H, Edwards N, Anderson CMH et al (2019) Trading amino acids at the aphid– Buchnera symbiotic interface. Proc Natl Acad Sci 116:16003–16011. https://doi.org/10.1073/pnas.1906223116
Fisher RM, Henry LM, Cornwallis CK et al (2017) The evolution of host-symbiont dependence. Nat Commun 8:1–8. https://doi.org/10.1038/ncomms15973
Foster KR, Schluter J, Coyte KZ, Rakoff-Nahoum S (2017) The evolution of the host microbiome as an ecosystem on a leash. Nature 548:43–51. https://doi.org/10.1038/nature23292
Frank SA (1996) Host-symbiont conflict over the mixing of symbiotic lineages. Proc R Soc B Biol Sci 263:339–344. https://doi.org/10.1098/rspb.1996.0052
Fronk DC, Sachs JL (2022) Symbiotic organs: the nexus of host–microbe evolution. Trends Ecol Evol 1–12. https://doi.org/10.1016/j.tree.2022.02.014
Garcia JR, Gerardo NM (2014) The symbiont side of symbiosis: do microbes really benefit? Front Microbiol 5:1–6. https://doi.org/10.3389/fmicb.2014.00510
Garcia JR, Larsen TJ, Queller DC, Strassmann JE (2019) Fitness costs and benefits vary for two facultative Burkholderia symbionts of the social amoeba, Dictyostelium discoideum. Ecol Evol 9:9878–9890. https://doi.org/10.1002/ece3.5529
Gavelis GS, Gile GH (2018) How did cyanobacteria first embark on the path to becoming plastids?: Lessons from protist symbioses. FEMS Microbiol Lett 365:1–11. https://doi.org/10.1093/femsle/fny209
Gerardo NM, Hoang KL, Stoy KS (2020) Evolution of animal immunity in the light of beneficial symbioses. Philos Trans R Soc London 375:20190601. https://doi.org/10.1098/rstb.2019.0601
Hamidou Soumana I, Berthier D, Tchicaya B et al (2013) Population dynamics of Glossina palpalis gambiensis symbionts, Sodalis glossinidius, and Wigglesworthia glossinidia, throughout host-fly development. Infect Genet Evol 13:41–48. https://doi.org/10.1016/j.meegid.2012.10.003
Haney EM, Huffman LH, Bougatsos C et al (2007) Screening for lipid disorders in children and adolescents: systematic evidence review for the U.S. Preventive Services Task Force. Evid Synth. https://doi.org/10.1001/jama.2023.11330
Hansen PJ, Moldrup M, Tarangkoon W et al (2012) Direct evidence for symbiont sequestration in the marine red tide ciliate Mesodinium rubrum. Aquat Microb Ecol 66:63–75. https://doi.org/10.3354/ame01559
Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mututalisms: Exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53
Hoang KL, Morran LT, Gerardo NM (2019) Can a symbiont (also) be food ? Front Microbiol 10:1–5. https://doi.org/10.3389/fmicb.2019.02539
Johnston PR, Rolff J (2015) Host and symbiont jointly control gut microbiota during complete metamorphosis. PLoS Pathog 1–11. https://doi.org/10.1371/journal.ppat.1005246
Kadono T, Kawano T, Hosoya H, Kosaka T (2004) Flow cytometric studies of the host-regulated cell cycle in algae symbiotic with green paramecium. Protoplasma 223:133–141. https://doi.org/10.1007/s00709-004-0046-6
Kereszt A, Mergaert P, Kondorosi E (2011) Bacteroid development in legume nodules: Evolution of mutual benefit or of sacrificial victims? Mol Plant-Microbe Interact 24:1300–1309. https://doi.org/10.1094/MPMI-06-11-0152
Kerwin AH, McAnulty SJ, Nyholm SV (2021) Development of the accessory nidamental gland and associated bacterial community in the hawaiian bobtail squid, euprymna scolopes. Biol Bull 240:205–218. https://doi.org/10.1086/713965
Kikuchi Y, Hosokawa T, Fukatsu T (2011) Specific developmental window for establishment of an insect-microbe gut symbiosis. Appl Environ Microbiol 77:4075–4081. https://doi.org/10.1128/AEM.00358-11
King KC (2019) Defensive symbionts. Curr Biol 29:R78–R80. https://doi.org/10.1016/j.cub.2018.11.028
Latef AAHA, Hashem A, Rasool S et al (2016) Arbuscular mycorrhizal symbiosis and abiotic stress in plants: A review. J Plant Biol 59:407–426. https://doi.org/10.1007/s12374-016-0237-7
Lau JA, Bowling EJ, Gentry LE et al (2012) Direct and interactive effects of light and nutrients on the legume-rhizobia mutualism. Acta Oecologica 39:80–86. https://doi.org/10.1016/j.actao.2012.01.004
Laurich JR, Dove R, Paillard C, Dufour SC (2018) Life and death in facultative chemosymbioses: control of bacterial population dynamics in the Thyasiridae. Symbiosis 75:123–133. https://doi.org/10.1007/s13199-017-0525-0
Law R, Dieckmann U (1998) Symbiosis through exploitation and the merger of lineages in evolution. Proc R Soc B 265:1245–1253
Law R, Lewis DH (1983) Biotic environments and the maintenance of sex–some evidence from mutualistic symbioses. Biol J Linn Soc 20:249–276. https://doi.org/10.1111/j.1095-8312.1983.tb01876.x
Lee KH, Ruby EG (1994) Effect of the squid host on the abundance and distribution of symbiotic Vibrio fischeri in nature. Appl Environ Microbiol 60:1565–1571. https://doi.org/10.1128/aem.60.5.1565-1571.1994
López-Madrigal S, Duarte EH (2020) Titer regulation in arthropod-Wolbachia symbioses. FEMS Microbiol Lett 366:1–9. https://doi.org/10.1093/femsle/fnz232
Lowe CD, Minter EJ, Cameron DD, Brockhurst MA (2016) Shining a light on exploitative host control in a photosynthetic endosymbiosis. Curr Biol 26:207–211. https://doi.org/10.1016/j.cub.2015.11.052
Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205. https://doi.org/10.1111/j.1365-2745.2008.01476.x
Margulis L, Fester R (eds) (1991) Symbiosis as a Source of Evolutionary Innovation: speciation and morphogenesis. MIT Press. https://mitpress.mit.edu/9780262519908/symbiosis-as-a-source-of-evolutionary-innovation/
McCutcheon JP, Boyd BM, Dale C (2019) The life of an insect endosymbiont from the cradle to the grave. Curr Biol 29:R485–R495. https://doi.org/10.1016/j.cub.2019.03.032
McFall-Ngai M (2008) Hawaiian bobtail squid. Curr Biol 18:1043–1044. https://doi.org/10.1016/j.cub.2008.08.059
McFall-Ngai MJ (2002) Unseen forces: the influence of bacteria on animal development. Dev Biol 14:1–14
Mendoza-Suárez MA, Geddes BA, Sánchez-Cañizares C et al (2020) Optimizing Rhizobium-legume symbioses by simultaneous measurement of rhizobial competitiveness and N2 fixation in nodules. Proc Natl Acad Sci USA 117:9822–9831. https://doi.org/10.1073/pnas.1921225117
Michonneau F, Brown JW, Winter DJ (2016) rotl: an R package to interact with the Open Tree of Life data. Methods Ecol Evol 7:1476–1481. https://doi.org/10.1111/2041-210X.12593
Motta MCM, Catta-Preta CMC, Schenkman S et al (2010) The bacterium endosymbiont of Crithidia deanei undergoes coordinated division with the host cell nucleus. PLoS ONE 5:20–21. https://doi.org/10.1371/journal.pone.0012415
Murfin KE, Lee M, Klassen JL et al (2015) Xenorhabdus bovienii strain diversity impacts coevolution and symbiotic maintenance with Steinernema spp. nematode hosts. Mbio 6:1–10. https://doi.org/10.1128/mBio.00076-15.Editor
Mushegian AA, Ebert D (2015) Rethinking “mutualism” in diverse host-symbiont communities. Bioessays 100–108. https://doi.org/10.1002/bies.201500074
Nishitani G, Nagai S, Hayakawa S et al (2012) Multiple plastids collected by the dinoflagellate Dinophysis mitra through kleptoplastidy. Appl Environ Microbiol 78:813–821. https://doi.org/10.1128/AEM.06544-11
Noble DWA, Lagisz M, O’dea RE, Nakagawa S (2017) Nonindependence and sensitivity analyses in ecological and evolutionary meta-analyses. Mol Ecol 26:2410–2425. https://doi.org/10.1111/mec.14031
O’brien AM, Sawers RJH, Ross-Ibarra J, Strauss SY (2018) Evolutionary responses to conditionality in species interactions across environmental gradients. Am Nat 192:715–730. https://doi.org/10.1086/700118
Oliver KM, Smith AH, Russell JA (2013) Defensive symbiosis in the real world - advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28:341–355. https://doi.org/10.1111/1365-2435.12133
Oono R, Anderson CG, Denison RF (2011) Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proc R Soc B Biol Sci 278:2698–2703. https://doi.org/10.1098/rspb.2010.2193
Paradis E, Schliep K (2019) Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35:526–528. https://doi.org/10.1093/bioinformatics/bty633
Pillet L, Pawlowski J (2013) Transcriptome analysis of foraminiferan elphidium margaritaceum questions the role of gene transfer in kleptoplastidy. Mol Biol Evol 30:66–69. https://doi.org/10.1093/molbev/mss226
Piquet B, Shillito B, Lallier FH et al (2019) High rates of apoptosis visualized in the symbiont-bearing gills of deep-sea Bathymodiolus mussels. PLoS ONE 14:1–21. https://doi.org/10.1371/journal.pone.0211499
Portal-Celhay C, Bradley ER, Blaser MJ (2012) Control of intestinal bacterial proliferation in regulation of lifespan in Caenorhabditis elegans. BMC Microbiol 12 https://doi.org/10.1186/1471-2180-12-49
R Core Team (2021) R: A language and environment for statistical computing. https://www.r-project.org/. Accessed 2021–2023
Revell LJ (2012) phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Rio RVM, Wu YN, Filardo G, Aksoy S (2006) Dynamics of multiple symbiont density regulation during host development: Tsetse fly and its microbial flora. Proc R Soc B Biol Sci 273:805–814. https://doi.org/10.1098/rspb.2005.3399
Rohatgi A (2021) Webplotdigitizer: Version 4.5. https://automeris.io/WebPlotDigitizer
Rumpho ME, Pelletreau KN, Moustafa A, Bhattacharya D (2011) The making of a photosynthetic animal. J Exp Biol 214:303–311. https://doi.org/10.1242/jeb.046540
Russell CW, Poliakov A, Haribal M et al (2014) Matching the supply of bacterial nutrients to the nutritional demand of the animal host. Proc R Soc B Biol Sci 281 https://doi.org/10.1098/rspb.2014.1163
Sachs JL, Essenberg CJ, Turcotte MM (2011) New paradigms for the evolution of beneficial infections. Trends Ecol Evol 26:202–209. https://doi.org/10.1016/j.tree.2011.01.010
Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science (80-) 310:1781. https://doi.org/10.1126/science.1120180
Schulte PM (2014) What is environmental stress? Insights from fish living in a variable environment. J Exp Biol 217:23–34. https://doi.org/10.1242/jeb.089722
Song C, Von Ahn S, Rohr RP, Saavedra S (2020) Towards a probabilistic understanding about the context-eependency of species interactions. Trends Ecol Evol 35:384–396. https://doi.org/10.1016/j.tree.2019.12.011
Sorensen MES, Lowe CD, Minter EJA et al (2019) The role of exploitation in the establishment of mutualistic microbial symbioses. FEMS Microbiol Lett 366:1–7. https://doi.org/10.1093/femsle/fnz148
Takahashi T (2016) Simultaneous evaluation of life cycle dynamics between a host Paramecium and the endosymbionts of Paramecium bursaria using capillary flow cytometry. Sci Rep 6:1–12. https://doi.org/10.1038/srep31638
Thomas MJ, Creed RP, Brown BL (2013) The effects of environmental context and initial density on symbiont populations in a freshwater cleaning symbiosis. Freshw Sci 32:1358–1366. https://doi.org/10.1899/12-187.1
Thutupalli S, Uppaluri S, Constable GWA et al (2017) Farming and public goods production in Caenorhabditis elegans populations. Proc Natl Acad Sci 114:2289–2294. https://doi.org/10.1073/pnas.1608961114
Uchiumi Y, Ohtsuki H, Sasaki A (2019) Evolution of self-limited cell division of symbionts. Proc R Soc B Biol Sci 286 https://doi.org/10.1098/rspb.2018.2238
Viechtbauer W (2010) Conducting meta-analyses in R with the metafor. J Stat Softw 36:1–48. https://doi.org/10.18637/jss.v036.i03
Vigneron A, Masson F, Vallier A et al (2014) Insects recycle endosymbionts when the benefit is over. Curr Biol 24:2267–2273. https://doi.org/10.1016/j.cub.2014.07.065
Weldon SR, Russell JA, Oliver KM (2019) More is not always better: coinfections with defensive symbionts generate highly variable outcomes. Appl Environ Microbiol 1–14 https://doi.org/10.1128/aem.02537-19
Weldon SR, Strand MR, Oliver KM (2013) Phage loss and the breakdown of a defensive symbiosis in aphids. Proc R Soc B 280:1–7. https://doi.org/10.1098/rspb.2012.2103
Whittle M, Bonsall MB, Barreaux AMG et al (2023) A theoretical model for host-controlled regulation of symbiont density. J Evol Biol 36:1731–1744. https://doi.org/10.1111/jeb.14246
Wollenberg MS, Ruby EG (2012) Phylogeny and fitness of Vibrio fischeri from the light organs of Euprymna scolopes in two Oahu, Hawaii populations. ISME J 6:352–362. https://doi.org/10.1038/ismej.2011.92
Wollenberg MS, Ruby EG (2009) Population structure of Vibrio fischeri within the light organs of Euprymna scolopes squid from two oahu (Hawaii) populations. Appl Environ Microbiol 75:193–202. https://doi.org/10.1038/ismej.2011.92
Wooldridge SA (2010) Is the coral-algae symbiosis really “mutually beneficial” for the partners? BioEssays 32:615–625. https://doi.org/10.1002/bies.200900182
Zhao D, Hoffmann AA, Zhang Z et al (2018) Interactions between Facultative Symbionts Hamiltonella and Cardinium in Bemisia tabaci (Hemiptera: Aleyrodoidea): Cooperation or Conflict? J Econ Entomol 111:2660–2666. https://doi.org/10.1093/jee/toy261
Acknowledgements
We are very grateful to Todd Palmer, Toby Kiers, and R. Ford Denison for providing the data from their respective studies. We thank Toby Kiers and Guillaume Chomicki for insightful feedback, the King lab for thoughtful discussion, and Pol Capdevila Lanzaco and Thomas Merrien for providing the codes for phylogenetic construction. KLH is supported by an NSF Postdoctoral Research Fellowship in Biology (1907076), RSG by a NERC Independent Research Fellowship (NE/M018458/1), VLP by a BBSRC Doctoral Training Grant (BB/M011224/1), and KCK by an ERC Starting Grant (COEVOPRO 802242) and NSERC Canada Excellence Research Chair.
Author information
Authors and Affiliations
Contributions
KLH and KCK conceptualized the topic. KLH collected and analyzed the data with input from KCK, RSG, and VLP. KLH wrote the original draft. All authors revised, edited, and approved the final version.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
13199_2024_984_MOESM1_ESM.docx
Supplementary file1 Figure S1. PRISMA flowchart of steps taken to identify studies to be used in host association, environmental, and time analyses. Figure S2. All effect sizes from eligible studies. Figure S3. Hosts, symbionts, and type of data included in analyses. Figure S4. Phylogenies of unculturable symbionts and their hosts. Table S1. Hosts and symbionts included in meta-analysis. Table S2. Closest relative to symbiont species included in meta-analysis. Table S3. Results of overall and moderator analyses, with all effect sizes or with outliers removed. (DOCX 1217 KB)
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Hoang, K.L., Salguero-Gómez, R., Pike, V.L. et al. The impacts of host association and perturbation on symbiont fitness. Symbiosis 92, 439–451 (2024). https://doi.org/10.1007/s13199-024-00984-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-024-00984-6