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Biology subjects

Montoya, J. M.

Publications and source records attributed to Montoya, J. M..

16 recordsLinked to original sources

Ocean depth modifies host-microbiome ecology and evolution

A major unsolved question in ecology and evolution is how similar free-living and symbiotic microbial communities are. In marine systems, depth homogenises free-living communities due to stronger dispersal and weaker environmental filtering compared to surface waters. We show that symbiotic communities of marine sponges follow a different pattern, with a subset of sponge species mirroring the increased similarity with depth seen in their free-living counterparts, while others remain highly host-specific both in shallow and deep waters. Moreover, in deep waters, more phylogenetically similar hosts harbor more similar microbiomes, yet host-symbiont cophylogeny nearly vanishes. This reveals two contrasting eco-evolutionary assembly rules: in more constant environments like the deep sea, community assembly is driven by host and environmental filtering with minimal signature of coevolution, whereas in variable environments, like shallow waters, host-symbiont coevolution is strong and key to maintain host-specific microbiomes.

microbiology↗

An eco-evolutionary theory of host-associated microbiomes

Host-associated microbiomes often display host specificity and heritability, yet the evolutionary processes under which such structured communities first emerge are still unclear. In particular, the conditions by which intergenerational (i.e. vertical) transmission of microbes can evolve and generate host-specific microbiomes are still unresolved. Here, we present an eco-evolutionary theory of microbiome assembly under minimal assumptions of microbial dynamics (i.e. neutrally driven by environmental fluctuations) and host control. We consider the adaptive evolution of microbial and host traits, including microbiome size and vertical transmission. We show that environmental fluctuations can generate enough among-host microbial variation to enable host-level selection favouring beneficial microbiome configurations. Vertical transmission can then evolve and, even when weak, allow microbiome specificity to be inherited and amplified across generations despite continuous influx from the external environment. Selection is most effective at intermediate levels of environmental fluctuation and host lifespan, revealing fundamental trade-offs between stochastic assembly, inheritance, and dispersal of microbes. The resulting microbiomes are dense, host-specific, and heritable, yet retain high intraspecific variability and lack strict phylosymbiosis. Simulated patterns of microbial dominance, diversity, and host-microbiome dissimilarity closely match those observed in nature, as evidenced using marine sponge microbiomes. Our results provide a mechanistic theory for the early evolution of host-associated microbiomes, showing that beneficial and species-specific communities can arise through selection and inheritance prior to the evolution of dedicated host-control mechanisms.

evolutionary biology↗

Towards key principles of host-associated microbiome assembly

Symbiotic relationships between microbes and host organisms frequently involve the assembly of complex microbial communities (microbiomes) within hosts. Patterns at the community level influence life-history traits, the evolutionary trajectories of both microbes and their hosts, and are often critical for maintaining host health. These community-level patterns are dynamically driven by eco-evolutionary mechanisms acting at the individual level, such as microbial dispersal, host selection, and microbe-resource interactions. Critically, we still lack a clear picture of the ways in which these mechanisms interact to shape microbiome assembly. Here, we present a model of assembly to describe how distinct community structures can be characterised by underlying mechanisms. To illustrate the approach, we analyse microbiome data from marine sponges and simulate different structures of host-microbe associations, thereby bridging mechanistic models and empirical patterns. We further apply the model to human microbiome data to explore its relevance across biological systems, proposing that the combined effect of a small set of general mechanisms may govern diverse patterns of microbial diversity and abundance. Our findings advance ecological theory by linking individual-level processes to community-scale patterns, illuminating the key drivers underlying microbiome assembly.

microbiology↗

Methylation dynamics in the decades preceding acute myeloid leukaemia

DNA methylation is emerging as a highly sensitive and specific marker of cancer initiation and progression. How these cancer-specific methylation changes are established in the decades before cancer, however, remains largely unknown. Here, we use a unique collection of longitudinal blood samples collected annually up to 15 years prior to a diagnosis of acute myeloid leukaemia to sensitively track the dynamics of DNA methylation changes at high temporal resolution. We identify thousands of differentially methylated regions (DMRs) that exhibit altered patterns of methylation up to 10 years before acute myeloid leukaemia (AML) diagnosis. Most of these DMRs are strongly associated with expanding clones carrying somatic driver mutations. We identify a subset of epigenetic driver DMRs characterised by recurrent CpG alterations that are highly shared across pre-AML cases. These are likely to reflect early epigenetic reprogramming associated with AML development. We also reveal large numbers of stochastic passenger CpGs whose differential methylation results from hitch-hiking with clonal expansions driven by somatically acquired genetic events. These passenger CpGs can be exploited for lineage tracing to discover clonal expansions driven by missing driver mutations. Our findings show widespread changes in methylation patterns during the early stages of cancer development which could be utilised for risk prediction and therapeutic intervention.

genomics↗

Thermal environment and ecological interactions modulate the importance of evolution in response to warming

Understanding the interaction between evolutionary history, the current abiotic environment, and biotic interactions is critical for a more nuanced understanding of the response of communities to anthropogenic stressors. We leveraged a long term experiment manipulating temperature in mesocosms containing communities of phytoplankton and zooplankton to examine how evolution in response to long-term community warming affects consumer-resource dynamics at different temperatures. We showed that the evolution in response to warming depends on both the current thermal environment, as well as the presence of interactions between consumers and resources. We also demonstrated that evolution influences the outcomes of current ecological dynamics. For each consumer-resource pair, the effects of evolution were temperature-dependent, but both the effects and the temperature dependence itself additionally depended upon the identity of evolving species in each pair. Evolution resulted on a win-win situation for the first resource species: across all temperatures, this resource was more fit and the consumer was less successful, with fitness gains peaking at intermediate temperatures. For this resource species our results supported the "hotter is better" hypothesis, especially at moderate or intermediate temperatures, while "hotter is worse" for the consumer. In the second species pair, patterns were more complex. Warm-origin populations of both the second resource and the consumer generally failed to show improved fitness. Overall, our results show that evolution altered resource and consumer fitness, but these effects were dependent on the current combination of abiotic and biotic conditions.

ecology↗

The effects of warming on the stability of consumer-resource interactions

Temperature regulates the physiology and behaviour of organisms. Thus, changing temperatures induce dynamics in species interactions. Considering that consumer-resource interactions underpin ecological communities, the impacts of warming on the stability of consumer-resource interactions have been extensively studied. However, a consensus among empirically determined warming-stability relationships and a clear understanding thereof is lacking. To investigate these systematically, we propose a simplified theoretical framework that can incorporate empirical data in three steps. First, we constrain stability to intrinsic oscillations to avoid comparing disparate stability notions. Second, we reduce complexity by utilising a one-dimensional stability metric. Third, we enable the direct comparison of all data by converting all thermal dependence parameterisations into a single function, with two parameters in the exponent determining its shape. The empirical data generate four different warming-stability relationships: stability increases, decreases, is hump-shaped or U-shaped with temperature. The diversity of warming-stability relationships, though partly attributable to context-dependence, is fundamentally caused by sensitivity to two factors: how the processes within the functional response are defined and the thermal dependence of carrying capacity. Consistency across studies regarding the former and acquiring more data on the latter should help uncover systematic patterns in the thermal dependence of stability in consumer-resource interactions.

ecology↗

Host Phylogeny Shapes Viral Transmission Networks in an Island Ecosystem

Viral transmission between host species underpins disease emergence. Both host phylogenetic relatedness and aspects of their ecology, such as species interactions and predator-prey relationships, may govern cross-species virus transmission and zoonotic risk, although their relative impact is unknown. By characterising the virome of a relatively isolated island ecological community linked through a food web we show that phylogenetic barriers result in distantly related host species sharing fewer viruses. Host ecology had a much smaller influence on overall virome composition. Network analysis revealed that hosts with a high diversity of viruses were more likely to gain new viruses, and that generalist viruses were more likely to infect new hosts. Such a highly connected ecological community heightens the risk of disease emergence, particularly among closely related species. One-Sentence SummarySequencing of an entire island virome reveals that closely related hosts have highly connected virus communities, increasing emergence risk.

microbiology↗

A framework to improve predictions of warming effects on consumer-resource interactions

Changes in temperature affect consumer-resource interactions, which underpin the functioning of ecosystems. However, existing studies report contrasting predictions regarding the impacts of warming on biological rates and community dynamics. To improve prediction accuracy and comparability, we develop an approach that combines sensitivity analysis and aggregate parameters. The former determines which biological parameters impact the community most strongly. The use of aggregate parameters (i.e., maximal energetic efficiency,{rho} , and interaction strength,{kappa} ), that combine multiple biological parameters, increases explanatory power and reduces the complexity of theoretical analyses. We illustrate the approach using empirically-derived thermal dependence curves of biological rates and applying it to consumer-resource biomass ratio and community stability. Based on our analyses, we generate four predictions: 1) resource growth rate regulates biomass distributions at mild temperatures, 2) interaction strength alone determines the thermal boundaries of the community, 3) warming destabilises dynamics at low and mild temperatures only, 4) interactions strength must decrease faster than maximal energetic efficiency for warming to stabilise dynamics. We argue for the potential benefits of directly working with the aggregate parameters to increase the accuracy of predictions on warming impacts on food webs and promote cross-system comparisons.

ecology↗

Warming indirectly increases invasion success in food webs

Climate warming and biological invasions are key drivers of biodiversity change. Their combined effects on ecological communities remain largely unexplored. We investigated the direct and indirect influences of warming on invasion success, and their synergistic effects on community structure and dynamics. Using size-structured food web models, we found that warming increased invasion success. The direct physiological effects of warming on invasions were minimal in comparison to indirect effects mediated by changes on food web structure and stability. Warmed communities with less connectivity, shortened food chains and reduced temporal variability were more susceptible to invasions. The directionality and magnitude of invasions effects on food webs varied across warming regimes. Warmer communities became smaller, more connected, and with more predator species when invaded than their colder counterparts. They were also less stable and their species more abundant. Considering food web structure is crucial to predict invasion success and its impacts under warming.

ecology↗

Intraspecific diversity loss in a predator species alters prey community structure and ecosystem functions

AO_SCPLOWBSTRACTC_SCPLOWLoss in intraspecific diversity can alter ecosystem functions, but the underlying mechanisms are still elusive, and intraspecific biodiversity-ecosystem function relationships (iBEF) have been restrained to primary producers. Here, we manipulated genetic and functional richness of a fish consumer (Phoxinus phoxinus), to test whether iBEF relationships exist in consumer species, and whether they are more likely sustained by genetic or functional richness. We found that both genotypic and functional richness affected ecosystem functioning, either independently or in interaction. Loss in genotypic richness reduced benthic invertebrate diversity consistently across functional richness treatments, whereas it reduced zooplankton diversity only when functional richness was high. Finally, both losses in genotypic and functional richness altered essential functions (e.g. decomposition) through trophic cascades. We concluded that iBEF relationships lead to substantial top-down effects on entire food chains. The loss of genotypic richness impacted ecological properties as much as the loss of functional richness, probably because it sustains "cryptic" functional diversity.

ecology↗

Temperature variability alters the stability and thresholds for collapse of interacting species

Temperature variability and extremes can have profound impacts on populations and ecological communities. Predicting impacts of thermal variability poses a challenge because it has both direct physiological effects and indirect effects through species interactions. In addition, differences in thermal performance between predators and prey and non-linear averaging of temperature-dependent performance can result in complex and counterintuitive population dynamics in response to climate change. Yet the combined consequences of these effects remain underexplored. Here, modeling temperature-dependent predator-prey dynamics, we study how changes in temperature variability affect population size, collapse, and stable coexistence of both predator and prey, relative to under constant environments or warming alone. We find that the effects of temperature variation on interacting species can lead to a diversity of outcomes, from predator collapse to stable coexistence, depending on interaction strengths and differences in species thermal performance. Temperature variability also alters predictions about population collapse - in some cases allowing predators to persist for longer than predicted when considering warming alone, and in others accelerating collapse. To inform management responses that are robust to future climates with increasing temperature variability and extremes, we need to incorporate the consequences of temperature variation in complex ecosystems.

ecology↗

Stoichiometric constraints modulate the effects of temperature and nutrients on biomass distribution and community stability

AO_SCPLOWBSTRACTC_SCPLOWTemperature and nutrients are two of the most important drivers of global change. Both can modify the elemental composition (i.e. stoichiometry) of primary producers and consumers. Yet their combined effect on the stoichiometry, dynamics, and stability of ecological communities remains largely unexplored. To fill this gap, we extended the Rosenzweig-MacArthur consumer-resource model by including thermal dependencies, nutrient dynamics, and stoichiometric constraints on both the primary producer and the consumer. We found that stoichiometric constraints dampen the paradox of enrichment and increased persistence at high nutrient levels. Nevertheless, they also reduced consumer persistence at extreme temperatures. Finally, we also found that stoichiometric constraints can strongly influence biomass distribution across trophic levels by modulating consumer assimilation efficiency and resource growth rates along the environmental gradients. In the Rosenzweig-MacArthur model, consumer biomass exceeded resource biomass for most parameter values whereas, in the stoichiometric model, consumer biomass was strongly reduced and sometimes lower than resource biomass. Our findings highlight the importance of accounting for stoichiometric constraints as they can mediate the temperature and nutrient impact on the dynamics and functioning of ecological communities.

ecology↗

Vertical transmission of sponge microbiota is weak and inconsistent

Classic coevolutionary theory predicts that if beneficial microbial symbionts improve host fitness, they should be faithfully transmitted to offspring. More recently, the hologenome theory of evolution predicts resemblance between parent and offspring microbiomes and high partner fidelity between host species and their vertically transmitted microbes. Here, we test these ideas for the first time in multiple coexisting host species with highly diverse microbiota, leveraging known parent-offspring pairs sampled from eight species of wild marine sponges (Porifera). We found that the processes governing vertical transmission were both neutral and selective. A neutral model explained 66% of the variance in larval microbiota, which was higher than the variance this model explained for adult sponge microbiota (R2 = 27%). However, microbes that are enriched above neutral expectations in adults were disproportionately transferred to offspring. Patterns of vertical transmission were, however, incomplete: larval sponges shared, on average, 44.8% of microbes with their parents, which was not higher than the fraction they shared with nearby non-parental adults. Vertical transmission was also inconsistent across siblings, as larval sponges from the same parent only shared 17% of microbes. Finally, we found no evidence that vertically transmitted microbes are faithful to a single sponge host species. Surprisingly, larvae were just as likely to share vertically transmitted microbes with larvae from other sponge species as they were with their own species. Our study demonstrates that common predictions of vertical transmission that stem from species-poor systems are not necessarily true when scaling up to diverse and complex microbiomes.

ecology↗

The Dynamic Core Microbiome: Structure, Stability And Resistance

The long-term stability of microbiomes is crucial as the persistent occurrence of beneficial microbes and their associated functions ensure host health and well-being. Microbiomes are highly diverse and dynamic, making them challenging to understand. Because many natural systems work as temporal networks, we present an approach that allows identifying meaningful ecological patterns within complex microbiomes: the dynamic core microbiome. On the basis of six marine sponge species sampled monthly over three years, we study the structure, dynamics and stability of their microbiomes. What emerge for each microbiome is a negative relationship between temporal variability and mean abundance. The notion of the dynamic core microbiome allowed us to determine a relevant functional attribute of the microbiome: temporal stability is not determined by the diversity of a hosts microbial assemblages, but rather by the density of those microbes that conform its core microbiome. The core microbial interaction network consisted of complementary members interacting weakly with dominance of comensal and amensal interactions that suggests self-regulation as a key determinant of the temporal stability of the microbiome. These interactions have likely coevolved to maintain host functionality and fitness over ecological, and even evolutionary time scales.

ecology↗

Uncovering The Drivers Of Animal-Host Microbiotas With Joint Distribution Modeling

In addition to the processes structuring free-living communities, host-associated microbiota are directly or indirectly shaped by the host. Therefore, microbiota data have a hierarchical structure where samples are nested under one or several variables representing host-specific factors, often spanning multiple levels of biological organization. Current statistical methods do not accommodate this hierarchical data structure, and therefore cannot explicitly account for the effect of the host in structuring the microbiota. We introduce a novel extension of joint species distribution models which can straightforwardly accommodate and discern between effects such as host phylogeny and traits, recorded covariates like diet and collection site, among other ecological processes. Our proposed methodology includes powerful yet familiar outputs seen in community ecology overall, including: (i) model-based ordination to visualize and quantify the main patterns in the data; (ii) variance partitioning to asses how influential the included host-specific factors are in structuring the microbiota; and (iii) co-occurrence networks to visualize microbe-to-microbe associations.

microbiology↗

Resilience, invariability, and ecological stability across levels of organization

Ecological stability is a bewildering broad concept. The most common stability measures are asymptotic resilience, widely used in theoretical studies, and measures based on temporal variability, commonly used in empirical studies. We construct measures of invariability, defined as the inverse of variability, that can be directly compared with asymptotic resilience. We show that asymptotic resilience behaves like the invariability of the most variable species, which is often a rare species close to its extinction boundary. Therefore, asymptotic resilience displays complete loss of stability with changes in community composition. In contrast, mean population invariability and ecosystem invariability are insensitive to rare species and quantify stability consistently whether details of species composition are considered or not. Invariability provides a consistent framework to predict diversity-stability relationships that agree with empirical data at population and ecosystem levels. Our findings can enhance the dialogue between theoretical and empirical stability studies.

ecology↗