Primate sympatry shapes the evolution of their brain architecture

The main hypotheses on the evolution of animal cognition emphasise the role of conspecifics in affecting the socio-ecological environment shaping cognition. Yet, space is often simultaneously occupied by multiple species from the same ecological guild. These sympatric species can compete for food, which may thereby stimulate or hamper cognition. Considering brain size as a proxy for cognition, we tested whether species sympatry impacted the evolution of cognition in frugivorous primates. We first retraced the evolutionary history of sympatry between frugivorous primate lineages. We then fitted phylogenetic models of the evolution of the size of several brain regions in frugivorous primates, considering or not species sympatry. We found that the evolution of the whole brain or brain regions used in immediate information processing was best fitted with models not considering sympatry. By contrast, models considering species sympatry best predicted the evolution of brain regions related to long-term memory of interactions with the socio-ecological environment, with a decrease in their size the higher the sympatry. We speculate that species sympatry, by generating intense food depletion, might lead to an over-complexification of resource spatiotemporality that counteracts the benefits of high cognitive abilities and/or might drive niche partitioning and specialisation, thereby inducing lower brain region sizes. In addition, we reported that primate species in sympatry diversify more slowly. This comparative study suggests that species sympatry significantly contributes to shaping primate evolution

Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks

Whether interactions between species are conserved on evolutionary time-scales has spurred the development of both correlative and process-based approaches for testing phylogenetic signal in interspecific interactions: do closely related species interact with similar partners? Here we use simulations to test the statistical performances of the two approaches that are the most widely used in the field: Mantel tests and the Phylogenetic Bipartite Linear Model (PBLM). Mantel tests investigate the correlation between phylogenetic distances and dissimilarities in sets of interacting partners, while PBLM is a process-based approach that relies on strong assumptions about how interactions evolve. We find that PBLM often detects a phylogenetic signal when it should not. Simple Mantel tests instead have infrequent false positives and moderate statistical power; however, they often artifactually detect that closely related species interact with dissimilar partners. Partial Mantel tests, which are used to partial out the phylogenetic signal in the number of partners, actually fail at correcting for this confounding effect, and we instead recommend evaluating the significance of Mantel tests with network permutations constraining the number of partners. We also explore the ability of simple Mantel tests to analyze clade-specific phylogenetic signals. We provide general guidelines and an application on an interaction network between orchids and mycorrhizal fungi.ecological network, phylogenetic signal, Mantel tests, clade-specific signal, species interactions, mycorrhizal symbiosis

Caractérisation et modélisation de l’évolution des interactions hôtes-microbiotes

De nombreuses études récentes ont permis de caractériser la composition des communautés microbiennes, appelées microbiotes, hébergées par plantes et animaux. Le but de ma thèse est de faire avancer notre compréhension de l’évolution des microbiotes associés aux espèces hôtes animales ou végétales, en utilisant comme données les arbres phylogénétiques des hôtes et des séquences d’ADN microbien de metabarcoding caractérisant leurs microbiotes. Pour cela, nous avons développé de nouvelles méthodes quantitatives, collecté des données ainsi que réalisé une série d’analyses. Nous avons considéré à la fois les microbes des animaux et des plantes, et tout particulièrement les interactions mycorhizennes. Dans le chapitre I, nous nous sommes intéressés à l’évolution du microbiote au cours de la diversification d’un clade d’hôtes. Nous avons développé une approche quantitative afin d’inférer les microbes transmis. À partir de la phylogénie des hôtes et de séquences d’ADN de leurs microbiotes, regroupées en unité taxonomique opérationnelle (OTU), notre approche utilise la variation nucléotidique au sein des OTUs pour détecter ceux qui sont transmis lors de la diversification des hôtes. Appliquée aux microbiotes de primates et araignées, nous avons trouvé que >5% des bactéries intestinales des primates étaient transmises verticalement, tandis qu’il n’y a vraisemblablement pas de transmission chez les araignées, confirmant l’hétérogénéité de l’évolution des interactions hôtes-microbes chez les animaux. Enfin, nous avons comparé les performances de notre modèle à celles d’autres approches existantes et montré que notre modèle est moins enclin aux faux-positifs lorsque la variation nucléotidique intra-OTU est faible. Dans le chapitre II, nous avons examiné les liens entre les histoires évolutives des hôtes et de leurs microbes associés. Nous avons plus particulièrement cherché à répondre à deux questions : « Dans quelle mesure les patrons d’interactions hôtes-microbiotes sont influencés par leurs histoires évolutives ? » et « comment l’histoire évolutive des hôtes influence-t-elle la diversification de leurs microbes associés ? ». La première question nous a amené à comparer les méthodes disponibles pour estimer le signal phylogénétique dans les réseaux d’interactions, afin de déterminer par exemple si des espèces de plantes proches ont tendance à interagir avec les mêmes champignons mycorhiziens. Nous avons trouvé qu’une approche fréquemment utilisée génère beaucoup de faux-positifs et qu’à l’inverse, les tests de Mantel donnent des résultats assez satisfaisants. Nous avons enfin exploré la seconde question en évaluant comment les plantes ont pu affecter la diversification des champignons endomycorhiziens (Glomeromycotina). Nos analyses suggèrent que ces symbiontes obligatoires ont récemment subit un ralentissement de leur diversification, qui peut être lié à l’évolution, chez de nombreuses plantes, de stratégies alternatives à l’endomycorhize. Dans le chapitre III, nous nous sommes focalisés sur l’évolution de la tricherie dans le mutualisme hôte-microbiote, et plus particulièrement dans la symbiose mycorhizienne. Nous avons exploré les contraintes limitant l’émergence de la tricherie chez les plantes (mycohétérotrophie) en analysant les patrons d’interactions endomycorhizennes à l’échelle mondiale. Nous avons ensuite étudié si des contraintes similaires s’appliquaient dans les communautés locales où vivent des plantes initialement mycohétérotrophes (les lycopodes), échantillonnées sur l’île de la Réunion. Nous en avons déduit qu’il existe généralement de fortes contraintes limitant la tricherie dans cette symbiose, mais que ces contraintes peuvent être relâchées au sein des communautés où la tricherie a lieu. Ainsi, ma thèse illustre que l’utilisation de méthodes quantitatives combinées à des données de metabarcoding, malgré leurs limites respectives, permet de mieux caractériser l’évolution des interactions hôtes-microbiotes.A plethora of recent studies have characterized the composition and functional role of microbial communities hosted by animals and plants, called microbiota. The overall goal of my PhD is to advance our understanding of how microbiota evolve with their host species, using data comprised of the phylogenetic relationships between host species and metabarcoding microbial sequences characterizing their microbial communities. We developed new quantitative tools, collected data, and performed a series of analyses, all directed to this common overarching goal. We considered both microbiota-animal and microbiota-plant systems, with a specific focus on mycorrhizal interactions. In Chapter I, we study the evolution of the microbiota during the diversification of host clades. We develop a quantitative approach for inferring the modes of microbial inheritance as host clades diversify. Given a host phylogeny and the microbiota of present-day species, each characterized by a list of short DNA sequences clustered into operational taxonomic units (OTUs), our approach uses nucleotide variability within OTUs to detect OTUs that are vertically transmitted. We apply this approach to two distinct systems, the gut microbiota of primates and a clade of Hawaiian spiders. We find that >5% of bacteria in primate guts are vertically transmitted, whereas there is no evidence of vertical transmission in spiders, confirming that host-microbiota evolutionary dynamics are highly heterogeneous across the animal kingdom. Finally, we compare the performances of our model to other available approaches and find that it is less prone to false-positives when the nucleotide variability within OTUs is low. In Chapter II, we examine the interplay between the evolutionary history of host and host-associated microbial clades. We focus on two specific questions: “To what extent does evolutionary history influence which microbial species interact with which host species?” and “How does the evolutionary history of hosts influence the diversification of host-associated microbial clades?”. The first question leads us to compare different methods for estimating phylogenetic signals in host-microbiota interactions, i.e. whether closely related species share similar sets of partners, with an application on plant-mycorrhizal interactions. We find that one of the most widely used approaches often detects phylogenetic signals when it should not and that Mantel tests perform best. We explore the second question by studying the diversification of the arbuscular mycorrhizal fungi (Glomeromycotina) in the past 500 million years and evaluating how land plants might have affected the diversification of these obligate mycorrhizal symbionts. Our analyses support that these fungi have experienced a recent diversification slowdown that might be linked to the shrinkage of their mycorrhizal niches as plant lineages evolve alternative symbiotic strategies. In Chapter III, we focus on the evolution of cheating in host-microbiota mutualisms, by taking the mycorrhizal symbiosis as a case study. We explore constraints on the evolutionary emergence of cheating in plants (mycoheterotrophy) by analyzing the patterns of plant-mycorrhizal fungus interactions at the global scale. Next, we investigate whether similar constraints are found in local mycorrhizal networks including initially mycoheterotrophic plants (Lycopodiaceae) that we have sampled in La Réunion island. We conclude that there are overall strong constraints limiting the emergence of cheaters in the mycorrhizal symbiosis, but these constraints might be relaxed in the local communities where cheating occurs. Overall, my thesis illustrates how new or recent computational tools, in combination with metabarcoding sequencing data, allow studying how microbiota evolve with their hosts. We discuss the challenges and promise of this comparative approach to host-microbiota evolution

Caractérisation et modélisation de l’évolution des interactions hôtes-microbiotes

A plethora of recent studies have characterized the composition and functional role of microbial communities hosted by animals and plants, called microbiota. The overall goal of my PhD is to advance our understanding of how microbiota evolve with their host species, using data comprised of the phylogenetic relationships between host species and metabarcoding microbial sequences characterizing their microbial communities. We developed new quantitative tools, collected data, and performed a series of analyses, all directed to this common overarching goal. We considered both microbiota-animal and microbiota-plant systems, with a specific focus on mycorrhizal interactions. In Chapter I, we study the evolution of the microbiota during the diversification of host clades. We develop a quantitative approach for inferring the modes of microbial inheritance as host clades diversify. Given a host phylogeny and the microbiota of present-day species, each characterized by a list of short DNA sequences clustered into operational taxonomic units (OTUs), our approach uses nucleotide variability within OTUs to detect OTUs that are vertically transmitted. We apply this approach to two distinct systems, the gut microbiota of primates and a clade of Hawaiian spiders. We find that >5% of bacteria in primate guts are vertically transmitted, whereas there is no evidence of vertical transmission in spiders, confirming that host-microbiota evolutionary dynamics are highly heterogeneous across the animal kingdom. Finally, we compare the performances of our model to other available approaches and find that it is less prone to false-positives when the nucleotide variability within OTUs is low. In Chapter II, we examine the interplay between the evolutionary history of host and host-associated microbial clades. We focus on two specific questions: “To what extent does evolutionary history influence which microbial species interact with which host species?” and “How does the evolutionary history of hosts influence the diversification of host-associated microbial clades?”. The first question leads us to compare different methods for estimating phylogenetic signals in host-microbiota interactions, i.e. whether closely related species share similar sets of partners, with an application on plant-mycorrhizal interactions. We find that one of the most widely used approaches often detects phylogenetic signals when it should not and that Mantel tests perform best. We explore the second question by studying the diversification of the arbuscular mycorrhizal fungi (Glomeromycotina) in the past 500 million years and evaluating how land plants might have affected the diversification of these obligate mycorrhizal symbionts. Our analyses support that these fungi have experienced a recent diversification slowdown that might be linked to the shrinkage of their mycorrhizal niches as plant lineages evolve alternative symbiotic strategies. In Chapter III, we focus on the evolution of cheating in host-microbiota mutualisms, by taking the mycorrhizal symbiosis as a case study. We explore constraints on the evolutionary emergence of cheating in plants (mycoheterotrophy) by analyzing the patterns of plant-mycorrhizal fungus interactions at the global scale. Next, we investigate whether similar constraints are found in local mycorrhizal networks including initially mycoheterotrophic plants (Lycopodiaceae) that we have sampled in La Réunion island. We conclude that there are overall strong constraints limiting the emergence of cheaters in the mycorrhizal symbiosis, but these constraints might be relaxed in the local communities where cheating occurs. Overall, my thesis illustrates how new or recent computational tools, in combination with metabarcoding sequencing data, allow studying how microbiota evolve with their hosts. We discuss the challenges and promise of this comparative approach to host-microbiota evolution.De nombreuses études récentes ont permis de caractériser la composition des communautés microbiennes, appelées microbiotes, hébergées par plantes et animaux. Le but de ma thèse est de faire avancer notre compréhension de l’évolution des microbiotes associés aux espèces hôtes animales ou végétales, en utilisant comme données les arbres phylogénétiques des hôtes et des séquences d’ADN microbien de metabarcoding caractérisant leurs microbiotes. Pour cela, nous avons développé de nouvelles méthodes quantitatives, collecté des données ainsi que réalisé une série d’analyses. Nous avons considéré à la fois les microbes des animaux et des plantes, et tout particulièrement les interactions mycorhizennes. Dans le chapitre I, nous nous sommes intéressés à l’évolution du microbiote au cours de la diversification d’un clade d’hôtes. Nous avons développé une approche quantitative afin d’inférer les microbes transmis. À partir de la phylogénie des hôtes et de séquences d’ADN de leurs microbiotes, regroupées en unité taxonomique opérationnelle (OTU), notre approche utilise la variation nucléotidique au sein des OTUs pour détecter ceux qui sont transmis lors de la diversification des hôtes. Appliquée aux microbiotes de primates et araignées, nous avons trouvé que >5% des bactéries intestinales des primates étaient transmises verticalement, tandis qu’il n’y a vraisemblablement pas de transmission chez les araignées, confirmant l’hétérogénéité de l’évolution des interactions hôtes-microbes chez les animaux. Enfin, nous avons comparé les performances de notre modèle à celles d’autres approches existantes et montré que notre modèle est moins enclin aux faux-positifs lorsque la variation nucléotidique intra-OTU est faible. Dans le chapitre II, nous avons examiné les liens entre les histoires évolutives des hôtes et de leurs microbes associés. Nous avons plus particulièrement cherché à répondre à deux questions : « Dans quelle mesure les patrons d’interactions hôtes-microbiotes sont influencés par leurs histoires évolutives ? » et « comment l’histoire évolutive des hôtes influence-t-elle la diversification de leurs microbes associés ? ». La première question nous a amené à comparer les méthodes disponibles pour estimer le signal phylogénétique dans les réseaux d’interactions, afin de déterminer par exemple si des espèces de plantes proches ont tendance à interagir avec les mêmes champignons mycorhiziens. Nous avons trouvé qu’une approche fréquemment utilisée génère beaucoup de faux-positifs et qu’à l’inverse, les tests de Mantel donnent des résultats assez satisfaisants. Nous avons enfin exploré la seconde question en évaluant comment les plantes ont pu affecter la diversification des champignons endomycorhiziens (Glomeromycotina). Nos analyses suggèrent que ces symbiontes obligatoires ont récemment subit un ralentissement de leur diversification, qui peut être lié à l’évolution, chez de nombreuses plantes, de stratégies alternatives à l’endomycorhize. Dans le chapitre III, nous nous sommes focalisés sur l’évolution de la tricherie dans le mutualisme hôte-microbiote, et plus particulièrement dans la symbiose mycorhizienne. Nous avons exploré les contraintes limitant l’émergence de la tricherie chez les plantes (mycohétérotrophie) en analysant les patrons d’interactions endomycorhizennes à l’échelle mondiale. Nous avons ensuite étudié si des contraintes similaires s’appliquaient dans les communautés locales où vivent des plantes initialement mycohétérotrophes (les lycopodes), échantillonnées sur l’île de la Réunion. Nous en avons déduit qu’il existe généralement de fortes contraintes limitant la tricherie dans cette symbiose, mais que ces contraintes peuvent être relâchées au sein des communautés où la tricherie a lieu. Ainsi, ma thèse illustre que l’utilisation de méthodes quantitatives combinées à des données de metabarcoding, malgré leurs limites respectives, permet de mieux caractériser l’évolution des interactions hôtes-microbiotes

Data on plant-fungus interactions in La Réunion island

This contains the OTU tables, the associated metadata, and the R script of the manuscript "Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities" by Perez-Lamarque B, Petrolli R, Strullu-Derrien C, Strasberg D, Morlon H, Selosse MA, Martos F. Environmental Microbiome 17, 38 (2022). https://doi.org/10.1186/s40793-022-00434-

Supplementary data on Glomeromycotina diversification

This contains the Supplementary Data of the manuscript "Analyzing diversification dynamics using barcoding data: the case of an obligate mycorrhizal symbiont" by Benoît Perez-Lamarque, Maarja Öpik, Odile Maliet, Ana C. Afonso Silva, Marc-André Selosse, Florent Martos, and Hélène Morlon. Molecular Ecology. 2022. https://doi.org/10.1111/mec.1647

Simulations of vertically transmitted OTUs

This contains simulated DNA alignment of microbial OTUs corresponding to microbes that are (i) vertically transmitted on the primate phylogeny, (ii) vertically transmitted with some events of horizontal host-switches, or (iii) independently evolving. It also contains both simulations performed without or with intra-host OTU duplications. For further details, see README.txt file or the Methods section of "Comparing different computational approaches for detecting long-term vertical transmission in host-associated microbiota" by Benoît Perez-Lamarque and Hélène Morlon

Characterizing symbiont inheritance during host–microbiota evolution: Application to the great apes gut microbiota

International audienceMicrobiota play a central role in the functioning of multicellular life, yet understanding their inheritance during host evolutionary history remains an important challenge. Symbiotic microorganisms are either acquired from the environment during the life of the host (i.e. environmental acquisition), transmitted across generations with a faithful association with their hosts (i.e. strict vertical transmission), or transmitted with occasional host switches (i.e. vertical transmission with horizontal switches). These different modes of inheritance affect microbes’ diversification, which at the two extremes can be independent from that of their associated host or follow host diversification. The few existing quantitative tools for investigating the inheritance of symbiotic organisms rely on cophylogenetic approaches, which require knowledge of both host and symbiont phylogenies, and are therefore often not well adapted to DNA metabarcoding microbial data. Here, we develop a model‐based framework for identifying vertically transmitted microbial taxa. We consider a model for the evolution of microbial sequences on a fixed host phylogeny that includes vertical transmission and horizontal host switches. This model allows estimating the number of host switches and testing for strict vertical transmission and independent evolution. We test our approach using simulations. Finally, we illustrate our framework on gut microbiota high‐throughput sequencing data of the family Hominidae and identify several microbial taxonomic units, including fibrolytic bacteria involved in carbohydrate digestion, that tend to be vertically transmitted