The Role of Multilevel Selection in Host Microbiome Evolution
Total Page：16
File Type：pdf, Size：1020Kb
The role of multilevel selection in host microbiome evolution Simon van Vlieta,1 and Michael Doebelia,b aDepartment of Zoology, University of British Columbia, Vancouver, BC V6T 1Z4, Canada; and bDepartment of Mathematics, University of British Columbia, Vancouver, BC V6T 1Z2, Canada Edited by W. Ford Doolittle, Dalhousie University, Halifax, Canada, and approved August 28, 2019 (received for review June 7, 2019) Animals are associated with a microbiome that can affect selection at the holobiont level is unlikely to play a major role in their reproductive success. It is, therefore, important to under- nature (13, 14, 17–19). stand how a host and its microbiome coevolve. According to the The strength of the association between a host and its micro- hologenome concept, hosts and their microbiome form an inte- biome is thus expected to depend on the relative importance grated evolutionary entity, a holobiont, on which selection can of vertical and horizontal transmission, and recent studies have potentially act directly. However, this view is controversial, and shown that organisms can vary strongly in this regard (11, 15). there is an active debate on whether the association between This raises the question for what organisms and under what hosts and their microbiomes is strong enough to allow for selec- conditions selection can act at the level of the holobiont. This tion at the holobiont level. Much of this debate is based on verbal question has been actively debated in the recent literature; how- arguments, but a quantitative framework is needed to investi- ever, most of this debate is based on verbal arguments (7–10, 13, gate the conditions under which selection can act at the holobiont 17, 18). In a recent model, the effects of horizontal and verti- level. Here, we use multilevel selection theory to develop such a cal transmission were studied for microbiomes consisting of only framework. We found that selection at the holobiont level can in a single genotype (11, 20). However, by excluding variation in principle favor a trait that is costly to the microbes but that pro- microbiome composition, this model could not address the ques- vides a benefit to the host. However, such scenarios require rather tion of under what conditions selection at the holobiont level can stringent conditions. The degree to which microbiome composi- maintain traits that are disfavored by selection at the microbe EVOLUTION tion is heritable decays with time, and selection can only act at level. This question is one of the most contentious points in the the holobiont level when this decay is slow enough, which occurs ongoing debate, and we address it here using a mathematical when vertical transmission is stronger than horizontal transmis- model. sion. Moreover, the host generation time has to be short enough We investigated under what conditions microbes can evolve compared with the timescale of the evolutionary dynamics at a trait that provides a benefit to the host but that comes at a the microbe level. Our framework thus allows us to quantita- cost to themselves. Such a trait is disfavored by selection at the tively predict for what kind of systems selection could act at the microbe level and can thus only evolve when selection can act at holobiont level. the holobiont level. We used a multilevel selection framework to address this question, as this allowed us to independently con- multilevel selection j microbiome j holobiont j hologenome trol the strength and direction of selection at both the microbe level and the host level. This multilevel selection framework does not explicitly incorporate the holobiont concept; however, asking ost multicellular organisms are associated with a micro- under what conditions holobiont-level selection can maintain a Mbiome that can strongly affect their health (1). For exam- ple, microbes residing in the animal gut can help digest food, provide essential nutrients, condition the immune system, and Significance even affect the mental health of their host (2–5). As a result, the reproductive success of a host often depends on the com- All animals carry microbes that can affect their health by pro- position of its microbiome (6). To understand the evolution of viding essential nutrients or other services. There is an active multicellular organisms, it is thus important to understand how debate about how hosts and their microbes coevolve. Specif- they coevolve with their microbiomes. ically, it is unclear when microbes can evolve altruistic traits Because of these strong interdependencies, some researchers that help their hosts but that come at a cost to themselves. have suggested that a host and its microbiome should be viewed Using a mathematical model, we show here that such traits as a single evolving entity, a so-called holobiont (7–11). Accord- can evolve but only under stringent conditions: hosts have to ing to this hologenome concept, selection can potentially act pass on their microbiome to their offspring, and their gener- directly at the level of the holobiont (7). As a result, traits that ation time has to be short. These conditions could potentially increase the overall reproductive success of a holobiont could occur in certain insect species but are unlikely to occur in long- evolve even if they are disfavored by selection at the level of the lived mammals. Our model thus allows us to predict in what microbes. types of hosts microbes could evolve altruistic traits. For selection to act at the level of the holobiont, it is essen- tial that there is an association between the genotype of a Author contributions: S.v.V. and M.D. designed research; S.v.V. performed research; S.v.V. host and the composition of its microbiome (12–14). Such an analyzed data; and S.v.V. and M.D. wrote the paper.y association could result from vertical transmission of the micro- The authors declare no conflicts of interest.y biome (i.e., when hosts pass a sample of their microbiome on This article is a PNAS Direct Submission.y to their offspring) (11, 15, 16). This vertical transmission creates Published under the PNAS license.y heritability in microbiome compositions, allowing hosts with suc- Data deposition: Code implemented in Python is available on Zenodo (https://doi.org/ cessful microbiomes to pass them on to their offspring. However, 10.5281/zenodo.3358236).y most hosts constantly take up microbes from their environ- 1 To whom correspondence may be addressed. Email: [email protected] ment, weakening the heritable association between a host and This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. its microbiome (11, 13, 15, 16). The pervasiveness of such hori- 1073/pnas.1909790116/-/DCSupplemental.y zontal transmission has led several researchers to conclude that www.pnas.org/cgi/doi/10.1073/pnas.1909790116 PNAS Latest Articles j 1 of 7 Downloaded by guest on October 2, 2021 trait that is opposed by microbe-level selection is equivalent to We assume that host birth rates increase linearly with the den- asking when host-level selection can maintain such a trait. Using sity of helper cells from β=GH in the absence of helper cells to simulations, we show that such a trait can evolve but only when (1 + sb ) · β=GH when a host is fully occupied by helper cells. vertical transmission is stronger than horizontal transmission and The parameter sb thus controls how strongly host birth rates when the host generation time is short enough compared with the depend on their microbiome. Similarly, we assume that host timescale of the evolutionary dynamics at the microbe level. death rates decrease linearly with the density of helper cells, with the parameter sd controlling the strength of this depen- Results dence (Fig. 1). Throughout the main text, we only consider the A Simple Model for Host–Microbe Evolutionary Dynamics. We case where helper cells increase host birth rates without affect- extended a previously developed multilevel selection framework ing host death rates (i.e., we assume that sd = 0). However, we (21) to investigate under what conditions selection can act at the obtained similar results when helper cells decreased host death host level. Throughout, we assumed the simplest possible dynam- rates instead (SI Appendix, Fig. S2). To maintain bounded host ics to reduce the number of model parameters. We consider a population sizes, we assume that host death rates are density microbiome consisting of 2 genotypes: helper cells and neutral dependent (Fig. 1). The generation times of hosts and microbes cells (Fig. 1). Helper and neutral cells are identical except for 1 typically differ strongly, and as a result, we expect evolutionary trait: helper cells increase the reproductive success of their host, change to happen at different timescales for hosts and microbes. but this comes at a cost to their own growth rate. We assume The parameter GH in our model controls how many microbial that microbes have a constant birth rate of β for the neutral cells generations occur within each host generation. and (1 − γ)β for the helper cells, where γ is the cost of helping. We explicitly incorporate the 2 modes of transmission, ver- We expect that, within a given host, microbes can grow to a maxi- tical and horizontal, in our model (Fig. 1). When a host gives mal population size, and thus assume that death rates are density birth, it passes a sample of its microbiome on to its offspring. T = n0 dependent (Fig. 1). Helper cells can transition into neutral cells The strength of vertical transmission vert k is measured and vice versa due to mutations. At each microbial division event, as the size of this sample n0 relative to the microbial carry- there is thus a probability µ that a microbe mutates to the other ing capacity k.