This study asks the central question: Is relatedness broadly predictive of the evolution of cooperation in microbes? Based on the data presented, what is the answer to this question? Do you think these findings are truly broad (meaning the same thing would be found in any other species)?
Kin selection explains the evolution of cooperation in the gut microbiota
Camille Simoneta,1 and Luke McNallya,b
a Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, United Kingdom; and b Centre for Synthetic and Systems Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3BF, United Kingdom
Edited by Joan E. Strassmann, Washington University in St. Louis, St. Louis, MO, and approved December 17, 2020 (received for review July 29, 2020)
Through the secretion of public goods molecules, microbes coop- eratively exploit their habitat. This is known as a major driver of the functioning of microbial communities, including in human dis- ease. Understanding why microbial species cooperate is therefore crucial to achieve successful microbial community management, such as microbiome manipulation. A leading explanation is that of Hamiltons inclusive-fitness framework. A cooperator can indirectly transmit its genes by helping the reproduction of an individual car- rying similar genes. Therefore, all else being equal, as relatedness among individuals increases, so should cooperation. However, the predictive power of relatedness, particularly in microbes, is sur- rounded by controversy. Using phylogenetic comparative analyses across the full diversity of the human gut microbiota and six forms of cooperation, we find that relatedness is predictive of the coop- erative gene content evolution in gut-microbe genomes. Hence, relatedness is predictive of cooperation over broad microbial tax- onomic levels that encompass variation in other life-history and ecology details. This supports the generality of Hamiltons central insights and the relevance of relatedness as a key parameter of interest to advance microbial predictive and engineering science.
cooperation | comparative analysis | microbiome |
evolutionary microbiology
anaging complex microbial communities (MCs) is key to a range of applications in the midst of our societys chal- lenges from microbiome manipulation (1) to sustainable food production (2) and climate regulation (3). The successful engi- neering of such communities requires the field of MCs and microbiome research to advance into more predictive science (4, 5). Crucial to this are theories of broad predictive ability. Firstly, such theories allow predictions that consistently hold across the vast diversity of microbial species making up those communities, and, secondly, they facilitate the translation of
theory into actionable tools.
Cooperative interactions are central to microbes lives, as well as how they interact with and modify their environment (613). Through the secretion of public goods, such as toxins, enzymes, or signaling molecules, microbes cooperatively exploit and mod- ify their habitat (14, 15). Recent omics studies have demon- strated the important role of such cooperative interactions in the evolution and function of real communities (16, 17), including diseases-associated communities (18). To predict and engineer the dynamics and evolution of MCs, it is therefore essential to understand the factors having a broad influence on the evolution of cooperation in the species making up these communities.
How cooperation evolves is puzzling because populations exhibiting such behavior are at risk from invasion by selfish cheats, reaping the reward without paying any of the cost (19). Hamiltons kin-selection theory provides an explanation: Even if sacrificing its own reproduction by helping a close relative reproduce, a cooperative individual can still pass on its genes to the next generation, albeit indirectly (20). Therefore, altruism is favored when fitness costs to the helper are overcome by benefits provided to the recipient weighted by their genetic relatedness (rb > c, Hamiltons rule). This gives a central role to genetic
relatedness, because it limits those indirect fitness benefits (21) (Fig. 1A). Hamiltons theory generates a prediction of great gen- erality: All else being equal, increased relatedness should lead to more cooperation. Contrary to predictions based on specific mechanisms [e.g., pleiotropy (22) or greenbeard genes (23, 24)] or that apply to a limited amount of taxa [e.g., particular sce- narios calling upon preadaptations (25, 26)], the generality of Hamiltons prediction is useful in that it identifies a unifying parameter (27). In the context of mastering MCs that are hugely diverse, such unifying principle is key. The question is then whether this is true in practice: Is relatedness broadly predictive of the evolution of cooperation in microbes?
Although kin selection has been a leading explanation for the evolution of cooperation from microorganisms to vertebrates in the field and in the laboratory (12, 13, 19, 23, 24, 2833), three main arguments cast doubt on its generality and predictive power in microbes. Firstly, even if relatedness drives cooperation, the direction of its effect may depend on the details of the biol- ogy of a particular cooperative behavior. For example, it has been shown that when a public good can be partly privatized (e.g., with strain-specific receptors), the public good becomes a competitive trait, therefore leading to a negative relationship between relatedness and the level of public-good production (34). Such variability in the direction of effect means that predic- tion may not be consistent across different types of cooperative behavior and species. Secondly, it has been suggested that inter- species interactions (i.e., when public goods provide interspecific
Author contributions: C.S. and L.M. designed research; C.S. performed research; C.S. analyzed data; and C.S. and L.M. wrote the paper.
The authors declare no competing interest. This article is a PNAS Direct Submission.
This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).
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1 To whom correspondence may be addressed. Email: [email protected].
This article contains supporting information online at https://www.pnas.org/lookup/suppl/ doi:10.1073/pnas.2016046118/-/DCSupplemental.
Published February 1, 2021.
PNAS 2021 Vol. 118 No. 6 e2016046118 https://doi.org/10.1073/pnas.2016046118 | 1 of 10
Fig. 1. Genetic relatedness in the human gut microbiome. (A) Schematic illustration of indirect fitness benefits. The cooperative cell loses the opportunity to produce c daughter cells (cost c). The help provided to the recipient cells allows them to each produce an additional b daughter cells (benefit b). The cooperative genes of the altruist cell are indirectly transmitted if the benefits provided enhance, on average, the reproduction of cells that also carry those cooperative genes, i.e., are genetically related; r > 0. (B) Methods schematic summary. Detailed within- and across-samples core genome size and nucleotide diversity are given in Dataset S1. SNPs, single-nucleotide polymorphisms. (C) Relatedness measures obtained for 101 species of the human gut microbiome. Vertical ticks are single point estimates of relatedness. The number of point estimates (i.e., number of hosts within which each species was found) is indicated on the right. The black dots represent the mean. Blue ticks are values between 25% and 75% quantiles.
benefit) may render relatedness unimportant at driving cooper- ation within species. This has been observed in the production of siderophores (a secreted iron-scavenging molecule acting as a public good) in Pseudomonas aeruginosa. In conditions such that siderophores also provided cross-species benefits (environment detoxification), the addition of a compost community allowed the growth of noncooperators, irrespective of the level of related- ness (35). This challenges the effective importance of relatedness
in real-world, complex communities. Third, theoretical work predicts that the population-genetics effects at work in the kin- selection framework may be unimportant in microbes owing to strong selection (25, 36, 37). Together, these arguments suggest that intraspecific relatedness may have minor or idiosyncratic effects on the evolution of cooperation in microbes.
Although these studies highlight potential limitations in the power of relatedness to predict the evolution of microbial
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Simonet and McNally
Kin selection explains the evolution of cooperation in the gut microbiota
