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Perez-Lamarque, B.

Publications and source records attributed to Perez-Lamarque, B..

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Evidence for a central ecological function of predatory Myxococcota in soil ecosystems

Myxococcota is a recently classified phylum including bacteria renowned for their predatory lifestyle. However, ecological functions of these bacteria remain under studied. Here, we examined the ecological position and potential impact of Myxococcota communities across diverse soil habitats using the global geographical collection of 16S microbial communities structured by the Earth Microbiome Project (EMP). First, we found that the abundance of Myxococcota varied greatly from 6.3% to 0.8% across 13 soil habitats. A deeper microbial analysis in two selected habitats showed that Myxococcota was highly abundant (4.9%) ranking 5 in field soil (a grassland planted with switchgrass) than in sand biofilter (an engineered system for water quality production, 1.3% and 11, resp.). Moreover, both Myxococcota and microbial communities displayed a significantly higher -diversity in field soil than in sand biofilter environments, suggesting that diversity of Myxococcota seems to be associated with that of microbial communities in these habitats. Using co-occurrence network analysis, we found that Myxococcota exhibited a high eigenvector centrality (5.1%) and one hub taxon, Polyangiales, in field soil habitat. In contrast, Myxococcota centrality was less pronounced (1.1%) in the sand biofilter, where consistent negative correlations were also detected. Altogether, these results suggest that Myxococcota communities experienced beneficial interactions in field soil environment, whereas they may have faced competitive relationships in sand biofilter habitat. Overall, our findings provide further insights into the status of Myxococcota communities in soil environments, suggesting their fundamental roles in the structure of soil microbial communities.

ecology↗

Darwin's entangled bank through deep time: Structural stability of mutualistic networks over evolutionary timescales

Mutualistic interactions form species-rich, complex networks that play essential roles for ecosystem function. Over macroevolutionary time scales, global- and continental-level networks change as species emerge and go extinct, yet the stability of their structural organization remains poorly understood. Here, we develop ELEFANT, a novel method for reconstructing ancestral interaction networks based on the hypothesis that species interactions are shaped by unobserved traits that evolve over evolutionary time. We show that ancestral interaction networks can be reliably reconstructed from present-day phylogenetic and interaction data. We infer the ancestral networks of plant mutualisms involving arbuscular mycorrhizal fungi, bat pollinators, and bird seed dispersers at large biogeographic scales. We find that these mutualistic networks exhibit a modular structure that seems to have persisted for millions of years, in part maintained by the evolutionary conservatism of species interactions. As species diversify, they tend to show limited shifts in mutualistic partners, which results in a remarkable long-term stability of mutualistic network structure at large spatial scales.

evolutionary biology↗

Questioning the Evidence for Host-Symbiont Codiversification in Mycorrhizal Symbioses

The vast majority of plants form mycorrhizal symbioses. The ecological importance of these mutualistic interactions has sparked interest in their long evolutionary history. By examining interaction networks and phylogenetic trees, several studies have suggested that plants codiversify with their associated mycorrhizal fungi. However, recent research has demonstrated that phylogenetic congruence (interpreted as codiversification when divergence times match) is often conflated with another pattern called cophylogenetic signal (i.e., closely related plants interacting with closely related fungi and vice versa), which may arise from different biological processes. We performed cophylogenetic analyses on 29 diverse mycorrhizal networks to reevaluate the evidence for codiversification in mycorrhizal symbioses. We found significant cophylogenetic signal but no phylogenetic congruence: closely related plants often interact with closely related fungi, but their phylogenies do not match. Instead of codiversification, this finding is consistent with trait matching between plants and mycorrhizal fungi, where compatible, evolutionarily conserved plant and fungal traits govern their interactions. Our work highlights the importance of appropriately interpreting the cophylogenetic methods used to study the macroevolution of plants and their mycorrhizal fungi. It suggests that previous evidence of codiversification in mycorrhizal symbioses actually detected cophylogenetic signal, since across the multiple and diverse networks analyzed here, there is no evidence that codiversification occurred during the evolution of mycorrhizal symbioses.

evolutionary biology↗

Orchids, hawkmoths and Darwin revisited: How adaptation to pollination by hawkmoths spurred the speciation of Old and New World angraecoids

Specialised pollination has often been proposed as a major driver of the unrivalled diversification of angiosperms. With its unparalleled variation in flower depth, ranging from spurless to 40 cm spurred flowers pollinated by hawkmoths, angraecoid orchids (Angraecinae) provide unique opportunities to reveal the impact of floral specialisation on diversification rates in the Afrotropics and Neotropics. We compiled floral characters for 327 angraecoid species, and assigned these species to newly formalised floral syndrome categories calibrated against pollination case studies. We then estimated ancestral character states and state-dependent speciation rates using the latest time-calibrated phylogeny of angraecoids. We found that white flowers consistent with micro-sphingophily (2 cm[&ge;] spurs <8.7 cm), macro-sphingophily (8.7 cm[&ge;] spurs <18.6 cm) and mega-sphingophily (spurs [&ge;]18.6 cm) evolved repeatedly in angraecoids, and are ancestral in some non-sphingophilous clades. Reversals to non-sphingophily and pigmented flowers suggest higher evolutionary lability of these traits than what is traditionally thought. Increasing floral specialisation with long spurs does not seem to enhance angraecoid orchids speciation rates, since micro-sphingophily appears to be associated with the highest speciation rates. An abundance of short-proboscid hawkmoths in Madagascar, as an ecological opportunity, may have accelerated the speciation of micro-sphingophilous taxa.

evolutionary biology↗

Factors shaping the assembly of lichen holobionts in a tropical lichen community

Lichen thalli host complex microbial communities, which may foster the ecological stability and longevity of the lichen symbiosis. Yet, we lack a holistic understanding of the processes contributing to the assembly of the lichen holobiont. This study assessed the diversity and community structure in taxonomically diverse co-occurring lichens associated with Trebouxiophyceae algae from Bolivian forests. We focused on three components of the lichen holobiont: the lichenized fungus (mycobiont) and its associated algae (photobiome) and fungi (mycobiome). We specifically tested the influence of mycobiont identity, thallus morphological type, reproductive strategy, and lichen secondary metabolites on the lichen-associated photobiome and mycobiome. To understand the specialization patterns between holobiont components, we investigated interaction networks. We observed that co-occurring mycobiont taxa host diverse, taxon-specific, yet overlapping photobiome and mycobiome. In particular, these communities are significantly influenced by the hosts thallus morphological type and its secondary metabolites. Finally, we demonstrated that both photobiome and mycobiome are structured mainly by mycobiont identity, which results in modular networks with strong phylogenetic signals and high levels of specialization. In conclusion, the symbiotic interactions within lichen are structured mainly by the mycobiont, which appears to be the leading architect of the lichen holobiont.

microbiology↗

Distinguishing cophylogenetic signal from phylogenetic congruence clarifies the interplay between evolutionary history and species interactions

Interspecific interactions, including host-symbiont associations, can profoundly affect the evolution of the interacting species. Given the phylogenies of host and symbiont clades and knowledge of which host species interact with which symbiont, two questions are often asked: "Do closely related hosts interact with closely related symbionts?" and "Do host and symbiont phylogenies mirror one another?". These questions are intertwined and can even collapse under specific situations, such that they are often confused one with the other. However, in most situations, a positive answer to the first question, hereafter referred to as "cophylogenetic signal", does not imply a close match between the host and symbiont phylogenies. It suggests only that past evolutionary history has contributed to shaping present-day interactions, which can arise, for example, through present-day trait matching, or from a single ancient vicariance event that increases the probability that closely related species overlap geographically. A positive answer to the second, referred to as "phylogenetic congruence", is more restrictive as it suggests a close match between the two phylogenies, which may happen, for example, if symbiont diversification tracks host diversification or if the diversifications of the two clades were subject to the same succession of vicariance events. Here we apply a set of methods (ParaFit, PACo, and eMPRess), which significance is often interpreted as evidence for phylogenetic congruence, to simulations under three biologically realistic scenarios of trait matching, a single ancient vicariance event, and phylogenetic tracking with frequent cospeciation events. The latter is the only scenario that generates phylogenetic congruence, whereas the first two generate a cophylogenetic signal in the absence of phylogenetic congruence. We find that tests of global-fit methods (ParaFit and PACo) are significant under the three scenarios, whereas tests of event-based methods (eMPRess) are only significant under the scenario of phylogenetic tracking. Therefore, significant results from global-fit methods should be interpreted in terms of cophylogenetic signal and not phylogenetic congruence; such significant results can arise under scenarios when hosts and symbionts had independent evolutionary histories. Conversely, significant results from event-based methods suggest a strong form of dependency between hosts and symbionts evolutionary histories. Clarifying the patterns detected by different cophylogenetic methods is key to understanding how interspecific interactions shape and are shaped by evolution.

evolutionary biology↗

Telling mutualistic and antagonistic ecological networks apart by learning their multiscale structure

O_LICharacterizing and understanding the processes that shape the structure of ecological networks, which represent who interacts with whom in a community, has many implications in ecology, evolutionary biology, and conservation. A highly debated question is whether and how the structure of a bipartite ecological network differs between antagonistic (e.g., herbivory) and mutualistic (e.g., pollination) interaction types. C_LIO_LIHere, we tackle this question by using a multiscale characterization of network structure, machine learning tools, and a large database of empirical and simulated bipartite networks. C_LIO_LIContrary to previous studies focusing on global structural metrics, such as nestedness and modularity, which concluded that antagonistic and mutualistic networks cannot be told apart from only their structure, we find that they can be told apart by combining a meso-scale characterization of their structure and supervised machine learning. Motif frequencies appear particularly informative, with an over-representation of densely connected motifs in antagonistic networks and of motifs with asymmetrical specialization in mutualistic networks. These characteristics can be used to predict interaction types with relatively good confidence. Beyond this classical mutualism/antagonism dichotomy, we also find significant structural uniqueness linked to specific ecologies (e.g., pollination, parasitism). C_LIO_LIOur results clarify structural differences between antagonistic and mutualistic networks and suggest the investigation of the structural uniqueness of specific ecologies as a promising approach for characterizing interactions beyond the coarse antagonistic/mutualistic dichotomy. C_LI

ecology↗

Recent evolutionary origin and localized diversity hotspots of mammalian coronaviruses

Several coronaviruses infect humans, with three, including the SARS-CoV2, causing diseases. While coronaviruses are especially prone to induce pandemics, we know little about their evolutionary history, host-to-host transmissions, and biogeography. One of the difficulties lies in dating the origination of the family, a particularly challenging task for RNA viruses in general. Previous cophylogenetic tests of virus-host associations, including in the Coronaviridae family, have suggested a virus-host codiversification history stretching many millions of years. Here, we establish a framework for robustly testing scenarios of ancient origination and codiversification versus recent origination and diversification by host switches. Applied to coronaviruses and their mammalian hosts, our results support a scenario of recent origination of coronaviruses in bats and diversification by host switches, with preferential host switches within mammalian orders. Hotspots of coronavirus diversity, concentrated in East Asia and Europe, are consistent with this scenario of relatively recent origination and localized host switches. Spillovers from bats to other species are rare, but have the highest probability to be towards humans than to any other mammal species, implicating humans as the evolutionary intermediate host. The high host-switching rates within orders, as well as between humans, domesticated mammals, and non-flying wild mammals, indicates the potential for rapid additional spreading of coronaviruses across the world. Our results suggest that the evolutionary history of extant mammalian coronaviruses is recent, and that cases of long-term virus-host codiversification have been largely over-estimated.

evolutionary biology↗

Phylogenetic comparative approach reveals evolutionary conservatism, ancestral composition, and integration of vertebrate gut microbiota

How host-associated microbial communities evolve as their hosts diversify remains equivocal: How conserved is their composition? What was the composition of ancestral microbiota? Do microbial taxa covary in abundance over millions of years? Multivariate phylogenetic models of trait evolution are key to answering similar questions for complex host phenotypes, yet they are not directly applicable to relative abundances, which usually characterize microbiota. Here, we extend these models in this context, thereby providing a powerful approach for estimating phylosymbiosis (the extent to which closely related host species harbor similar microbiota), ancestral microbiota composition, and integration (evolutionary covariations in bacterial abundances). We apply our model to the gut microbiota of mammals and birds. We find significant phylosymbiosis that is not entirely explained by diet and geographic location, indicating that other evolutionary-conserved traits shape microbiota composition. We identify main shifts in microbiota composition during the evolution of the two groups and infer an ancestral mammalian microbiota consistent with an insectivorous diet. We also find remarkably consistent evolutionary covariations among bacterial orders in mammals and birds. Surprisingly, despite the substantial variability of present-day gut microbiota, some aspects of their composition are conserved over millions of years of host evolutionary history.

evolutionary biology↗

Gains and losses of the epiphytic lifestyle in epidendroid orchids: review and new analyses with succulence traits

Background and AimsEpiphytism has evolved repeatedly in plants and has resulted in a considerable number of species with original characteristics. Succulent forms in particular are thought to have evolved as an adaptation to the epiphytic environment, because the water supply is generally erratic compared to soils. However, succulent organs also exist in terrestrial plants, and the question of the concomitant evolution of epiphytism and succulence has received little attention, not even in the epidendroid orchids, which account for 68% of vascular epiphytes. MethodsWe reconstructed a new time-calibrated phylogenetic tree of Epidendroideae with 203 genera treated in Genera Orchidacearum, from which we reconstructed the evolution of epiphytism and other traits including stem and leaf succulence, while testing the correlated evolution between lifestyle and morphological traits. Furthermore, we reconstructed the ancestral geographic ranges to interpret major character changes during the Cenozoic. Key ResultsEpiphytism evolved at least 7.1 My ago in the neotropical Sobralieae, 11.5 My ago in the Arethuseae in Southeast Asia and Australia, and 39.0 My ago in the common ancestor of the Dendrobieae and Cymbidieae in the three previous areas, and was notably lost in the Malaxideae, Collabieae, Calypsoeae, Bletiinae, and Eulophiinae. Stem succulence is inferred to have evolved once, in a terrestrial ancestor 43.1 My ago, thus preceding the evolution of epiphytism by at least 4.1 My. If lost, stem succulence was almost systematically replaced by leaf succulence in epiphytic lineages. ConclusionsEpiphytism probably evolved from terrestrial orchids already possessing succulent stems, which appeared during Eocene climatic cooling. Both epiphytic and secondary terrestrial Epidendroideae may have appeared in seasonally-dry forests. Thus, we believe that the emergence of stem succulence in early epidendroids was a key innovation in the evolution of orchids, facilitating the colonisation of epiphytic environments that led to the greatest diversification of orchids.

evolutionary biology↗

Comparing different computational approaches for detecting long-term vertical transmission in host-associated microbiota

Long-term vertical transmissions of gut bacteria are thought to be frequent and functionally important in mammals. Several phylogenetic-based approaches have been proposed to detect, among species-rich microbiota, the bacteria that have been vertically transmitted during a host clade radiation. Applied to mammal microbiota, these methods have sometimes led to conflicting results; in addition, how they cope with the slow evolution of markers typically used to characterize bacterial microbiota remains unclear. Here, we use simulations to test the statistical performances of two widely-used global-fit approaches (ParaFit and PACo) and two event-based approaches (ALE and HOME). We find that these approaches have different strengths and weaknesses depending on the amount of variation in the bacterial DNA sequences and are therefore complementary. In particular, we show that ALE performs better when there is a lot of variation in the bacterial DNA sequences, whereas HOME performs better when there is not. Global-fit approaches (ParaFit and PACo) have higher type-I error rates (false positives) but have the advantage to be very fast to run. We apply these methods to the gut microbiota of primates and our results suggest that only a small fraction of their gut bacteria is vertically transmitted.

evolutionary biology↗

Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities

BackgroundThe root mycobiome plays a fundamental role in plant nutrition and protection against biotic and abiotic stresses. In temperate forests or meadows dominated by angiosperms, the numerous fungi involved in root symbioses are often shared between neighboring plants, thus forming complex plant-fungus interaction networks of weak specialization. Whether this weak specialization also holds in rich tropical communities with more phylogenetically diverse sets of plant lineages remains unknown. We collected roots of 30 plant species in semi-natural tropical communities including angiosperms, ferns, and lycophytes, in three different habitat types on La Reunion island: a recent lava flow, a wet thicket, and an ericoid shrubland. We identified root-inhabiting fungi by sequencing both the 18S rRNA and the ITS2 variable regions. We assessed the diversity of mycorrhizal fungal taxa according to plant species and lineages, as well as the structure and specialization of the resulting plant-fungus networks. ResultsThe 18S and ITS2 datasets are highly complementary at revealing the root mycobiota. According to 18S, Glomeromycotina colonize all plant groups in all habitats forming the least specialized interactions, resulting in nested network structures, while Mucoromycotina (Endogonales) are more abundant in the wetland and show higher specialization and modularity compared to the former. According to ITS2, mycorrhizal fungi of Ericaceae and Orchidaceae, namely Helotiales, Sebacinales, and Cantharellales, also colonize the roots of most plant lineages, confirming that they are frequent endophytes. While Helotiales and Sebacinales present intermediate levels of specialization, Cantharellales are more specialized and more sporadic in their interactions with plants, resulting in highly modular networks. ConclusionsThis study of the root mycobiome in tropical environments reinforces the idea that mycorrhizal fungal taxa are locally shared between co-occurring plants, including phylogenetically distant plants (e.g. lycophytes and angiosperms), where they may form functional mycorrhizae or establish endophytic colonization. Yet, we demonstrate that, irrespectively of the environmental variations, the level of specialization significantly varies according to the fungal lineages, probably reflecting the different evolutionary origins of these plant-fungus symbioses. Frequent fungal sharing between plants questions the roles of the different fungi in community functioning and highlights the importance of considering networks of interactions rather than isolated hosts.

ecology↗

Species sympatry shapes brain size evolution in Primates

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.

ecology↗

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

AO_SCPLOWBSTRACTC_SCPLOWWhether 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.

ecology↗

A holobiont view of island biogeography: unraveling patterns driving the nascent diversification of a Hawaiian spider and its microbial associates

The diversification of a host lineage can be influenced by both the external environment and its assemblage of microbes. Here, we use a young lineage of spiders, distributed along a chronologically arranged series of volcanic mountains, to determine the parallels between the evolutionary histories of the host spiders and their associated microbial communities, together forming the "holobiont". Using the stick spider Ariamnes waikula (Araneae, Theridiidae) on the island of Hawaii, and outgroup taxa on older islands, we tested whether each component of the holobiont (the spider hosts, the intracellular endosymbionts, and the gut microbial communities) showed correlated signatures of diversity due to sequential colonization from older to younger volcanoes. In order to investigate this, we generated ddRAD data for the host spiders and 16S rRNA gene amplicon data from their microbiota. We expected sequential colonizations to result in a (phylo)genetic structuring of the host spiders and in a diversity gradient in microbial communities. Results showed that the host A. waikula is indeed structured by geographic isolation, suggesting sequential colonization from older to younger volcanoes. Similarly, the endosymbiont communities were markedly different between Ariamnes species on different islands, but more homogeneous among A. waikula populations on the island of Hawaii. Conversely, the gut microbiota was largely conserved across all populations and species, which we suspect are generally environmentally derived. Our results highlight that the different components of the holobiont have responded in distinct ways to the dynamic environment of the volcanic archipelago, showing the necessity of understanding the interplay between components to better characterize holobiont evolution.

evolutionary biology↗

Diversification slowdown in an evolutionary cul-de-sac

Analyzing diversification dynamics is key to understanding the past evolutionary history of clades that led to present-day biodiversity patterns. While such analyses are widespread in well-characterized groups of species, they are much more challenging in groups which diversity is mostly known through molecular techniques. Here, we use the largest global database on the small subunit (SSU) rRNA gene of Glomeromycotina, a subphylum of microscopic arbuscular mycorrhizal fungi that provide mineral nutrients to most land plants by forming one of the oldest terrestrial symbioses, to analyze the diversification dynamics of this clade in the past 500 million years (Myr). We perform a range of sensitivity analyses and simulations to control for potential biases linked to the nature of the data. We find that Glomeromycotina tend to have low speciation rates compared to other eukaryotes. After a peak of speciations between 200 and 100 Myr ago, they experienced an important decline in speciation rates toward the present. Such a decline could be at least partially related to a shrinking of their mycorrhizal niches and to their limited ability to colonize new niches. Our analyses identify patterns of diversification in a group of obligate symbionts of major ecological and evolutionary importance and illustrate that short molecular markers combined with intensive sensitivity analyses can be useful for studying diversification dynamics in microbial groups.

evolutionary biology↗

Constraints upon cheating emergence in mutualistic networks: evidence in the mycorrhizal symbiosis

O_LIWhile mutualisms are widespread and essential in ecosystem functioning, the emergence of uncooperative cheaters threatens their stability, unless there are functional or evolutionary mechanisms limiting cheaters interactions.\nC_LIO_LIHere, we evaluated the constraints upon mycoheterotrophic (MH) cheating plants in the mutualistic interaction network of autotrophic (AT) plants and arbuscular mycorrhizal fungi. For this purpose, we assembled a world-scale network of >25,000 interactions in order to investigate (i) the specialization and (ii) the phylogenetic distribution of MH or AT plants and their respective fungal partners.\nC_LIO_LIWe show that MH cheating repeatedly evolved in the vascular flora, suggesting low phylogenetic constraint for plants. However, MH cheaters are significantly more specialized than AT plants, and their fungi also appear more specialized and more closely related than fungi of AT plants, which suggest that cheaters are specifically isolated into modules by functional constraints\nC_LIO_LIThis unprecedented comparison of MH vs. AT plants thus reveals that MH cheating is most likely constrained by the specialization of phylogenetically conserved cheating-susceptible fungi, which suggests mechanisms for avoidance of these fungi. Beyond the mycorrhizal symbiosis, our approach highlights an empirical multiple-partners mutualistic system illustrating that the overall persistence of mutualism can be linked to functional constraints upon cheating emergences.\nC_LI

evolutionary biology↗