Chewing through challenges: Exploring the evolutionary pathways to wood-feeding in insects.

Decaying wood, while an abundant and stable resource, presents considerable nutritional challenges due to its structural rigidity, chemical recalcitrance, and low nitrogen content. Despite these challenges, certain insect lineages have successfully evolved saproxylophagy (consuming and deriving sustenance from decaying wood), impacting nutrient recycling in ecosystems and carbon sequestration dynamics. This study explores the uneven phylogenetic distribution of saproxylophagy across insects and delves into the evolutionary origins of this trait in disparate insect orders. Employing a comprehensive analysis of gut microbiome data, from both saproxylophagous insects and their non-saproxylophagous relatives, including new data from unexplored wood-feeding insects, this Hypothesis paper discusses the broader phylogenetic context and potential adaptations necessary for this dietary specialization. The study proposes the "Detritivore-First Hypothesis," suggesting an evolutionary pathway to saproxylophagy through detritivory, and highlights the critical role of symbiotic gut microbiomes in the digestion of decaying wood.

Strong connectivity in real directed networks.

In many real, directed networks, the strongly connected component of nodes which are mutually reachable is very small. This does not fit with current theory, based on random graphs, according to which strong connectivity depends on mean degree and degree-degree correlations. And it has important implications for other properties of real networks and the dynamical behavior of many complex systems. We find that strong connectivity depends crucially on the extent to which the network has an overall direction or hierarchical ordering-a property measured by trophic coherence. Using percolation theory, we find the critical point separating weakly and strongly connected regimes and confirm our results on many real-world networks, including ecological, neural, trade, and social networks. We show that the connectivity structure can be disrupted with minimal effort by a targeted attack on edges which run counter to the overall direction. This means that many dynamical processes on networks can depend significantly on a small fraction of edges.

Choanoflagellates alongside diverse uncultured predatory protists consume the abundant open-ocean cyanobacterium Prochlorococcus.

Prochlorococcus is a key member of open-ocean primary producer communities. Despite its importance, little is known about the predators that consume this cyanobacterium and make its biomass available to higher trophic levels. We identify potential predators along a gradient wherein Prochlorococcus abundance increased from near detection limits (coastal California) to >200,000 cells mL-1 (subtropical North Pacific Gyre). A replicated RNA-Stable Isotope Probing experiment involving the in situ community, and labeled Prochlorococcus as prey, revealed choanoflagellates as the most active predators of Prochlorococcus, alongside a radiolarian, chrysophytes, dictyochophytes, and specific MAST lineages. These predators were not appropriately highlighted in multiyear conventional 18S rRNA gene amplicon surveys where dinoflagellates and other taxa had highest relative amplicon abundances across the gradient. In identifying direct consumers of Prochlorococcus, we reveal food-web linkages of individual protistan taxa and resolve routes of carbon transfer from the base of marine food webs.

Experimentally simulating the evolution-to-ecology connection: Divergent predator morphologies alter natural food webs.

The idea that changing environmental conditions drive adaptive evolution is a pillar of evolutionary ecology. But, the opposite-that adaptive evolution alters ecological processes-has received far less attention yet is critical for eco-evolutionary dynamics. We assessed the ecological impact of divergent values in a key adaptive trait using 16 populations of the brown anole lizard (Anolis sagrei). Mirroring natural variation, we established islands with short- or long-limbed lizards at both low and high densities. We then monitored changes in lower trophic levels, finding that on islands with a high density of short-limbed lizards, web-spider densities decreased and plants grew more via an indirect positive effect, likely through an herbivore-mediated trophic cascade. Our experiment provides strong support for evolution-to-ecology connections in nature, likely closing an otherwise well-characterized eco-evolutionary feedback loop.

Top predator sea stars are the benthic equivalent to polar bears of the pelagic realm.

The marine pelagic compartment spans numerous trophic levels and consists of numerous reticulate connections between species from primary producers to iconic apex predators, while the benthic compartment is perceived to be simpler in structure and comprised of only low trophic level species. Here, we challenge this paradigm by illustrating that the benthic compartment is home to a subweb of similar structure and complexity to that of the pelagic realm, including the benthic equivalent to iconic polar bears: megafaunal-predatory sea stars.

Sex-biased effects on hippocampal circuit development by perinatal SERT expression in CA3 pyramidal neurons.

Neurodevelopmental disorders ranging from autism to intellectual disability display sex-biased prevalence and phenotypical presentations. Despite increasing knowledge about temporospatial cortical map development and genetic variants linked to neurodevelopmental disorders, when and how sex-biased neural circuit derailment may arise in diseased brain remain unknown. Here, we identify in mice that serotonin uptake transporter (SERT) in non-serotonergic neurons - hippocampal and prefrontal pyramidal neurons - confers sex-biased effects specifically during neural circuit development. A set of gradient-patterned CA3 pyramidal neurons transiently express SERT to clear extracellular serotonin, coinciding with hippocampal synaptic circuit establishment. Ablating pyramidal neuron SERT (SERTPyramidΔ) alters dendritic spine developmental trajectory in the hippocampus, and precipitates sex-biased impairments in long-term activity-dependent hippocampal synaptic plasticity and cognitive behaviors. Transcriptomic analyses identify sex-biased alterations in gene sets associated with autism, dendritic spine structure, synaptic function and male-specific enrichment of dysregulated genes in glial cells in early postnatal SERTPyramidΔ hippocampus. Our data suggest that SERT function in these pyramidal neurons underscores a temporal- and brain region-specific regulation of normal sex-dimorphic circuit development and a source for sex-biased vulnerability to cognitive and behavioral impairments. This article has an associated 'The people behind the papers' interview.

A Rapid Induction Mechanism for Lin28a in Trophic Responses.

Environmental cues provoke rapid transitions in gene expression to support growth and cellular plasticity through incompletely understood mechanisms. Lin28 RNA-binding proteins have evolutionarily conserved roles in post-transcriptional coordination of pro-growth gene expression, but signaling pathways allowing trophic stimuli to induce Lin28 have remained uncharacterized. We find that Lin28a protein exhibits rapid basal turnover in neurons and that mitogen-activated protein kinase (MAPK)-dependent phosphorylation of the RNA-silencing factor HIV TAR-RNA-binding protein (TRBP) promotes binding and stabilization of Lin28a, but not Lin28b, with an accompanying reduction in Lin28-regulated miRNAs, downstream of brain-derived neurotrophic factor (BDNF). Binding of Lin28a to TRBP in vitro is also enhanced by phospho-mimic TRBP. Further, phospho-TRBP recapitulates BDNF-induced neuronal dendritic spine growth in a Lin28a-dependent manner. Finally, we demonstrate MAPK-dependent TRBP and Lin28a induction, with physiological function in growth and survival, downstream of diverse growth factors in multiple primary cell types, supporting a broad role for this pathway in trophic responses.

Trophic interactions with heterotrophic bacteria limit the range of Prochlorococcus.

Prochlorococcus is both the smallest and numerically most abundant photosynthesizing organism on the planet. While thriving in the warm oligotrophic gyres, Prochlorococcus concentrations drop rapidly in higher-latitude regions. Transect data from the North Pacific show the collapse occurring at a wide range of temperatures and latitudes (temperature is often hypothesized to cause this shift), suggesting an ecological mechanism may be at play. An often used size-based theory of phytoplankton community structure that has been incorporated into computational models correctly predicts the dominance of Prochlorococcus in the gyres, and the relative dominance of larger cells at high latitudes. However, both theory and computational models fail to explain the poleward collapse. When heterotrophic bacteria and predators that prey nonspecifically on both Prochlorococcus and bacteria are included in the theoretical framework, the collapse of Prochlorococcus occurs with increasing nutrient supplies. The poleward collapse of Prochlorococcus populations then naturally emerges when this mechanism of "shared predation" is implemented in a complex global ecosystem model. Additionally, the theory correctly predicts trends in both the abundance and mean size of the heterotrophic bacteria. These results suggest that ecological controls need to be considered to understand the biogeography of Prochlorococcus and predict its changes under future ocean conditions. Indirect interactions within a microbial network can be essential in setting community structure.

Emergent effects of global change on consumption depend on consumers and their resources in marine systems.

A better understanding of how environmental change will affect species interactions would significantly aid efforts to scale up predictions of near-future responses to global change from individuals to ecosystems. To address this need, we used meta-analysis to quantify the individual and combined effects of ocean acidification (OA) and warming on consumption rates of predators and herbivores in marine ecosystems. Although the primary studies demonstrated that these environmental variables can have direct effects on consumers, our analyses highlight high variability in consumption rates in response to OA and warming. This variability likely reflects differences in local adaptation among species, as well as important methodological differences. For example, our results suggest that exposure of consumers to OA reduces consumption rates on average, yet consumption rates actually increase when both consumers and their resource(s) are concurrently exposed to the same conditions. We hypothesize that this disparity is due to increased vulnerability of prey or resource(s) in conditions of OA that offset declines in consumption. This hypothesis is supported by an analysis demonstrating clear declines in prey survival in studies that exposed only prey to future OA conditions. Our results illustrate how simultaneous OA and warming produce complex outcomes when species interact. Researchers should further explore other potential sources of variation in response, as well as the prey-driven component of any changes in consumption and the potential for interactive effects of OA and warming.

Sublethal effects of parasitism on ruminants can have cascading consequences for ecosystems.

Parasitic infections are common, but how they shape ecosystem-level processes is understudied. Using a mathematical model and meta-analysis, we explored the potential for helminth parasites to trigger trophic cascades through lethal and sublethal effects imposed on herbivorous ruminant hosts after infection. First, using the model, we linked negative effects of parasitic infection on host survival, fecundity, and feeding rate to host and producer biomass. Our model, parameterized with data from a well-documented producer­caribou­helminth system, reveals that even moderate impacts of parasites on host survival, fecundity, or feeding rate can have cascading effects on ruminant host and producer biomass. Second, using meta-analysis, we investigated the links between helminth infections and traits of free-living ruminant hosts in nature. We found that helminth infections tend to exert negative but sublethal effects on ruminant hosts. Specifically, infection significantly reduces host feeding rates, body mass, and body condition but has weak and highly variable effects on survival and fecundity. Together, these findings suggest that while helminth parasites can trigger trophic cascades through multiple mechanisms, overlooked sublethal effects on nonreproductive traits likely dominate their impacts on ecosystems. In particular, by reducing ruminant herbivory, pervasive helminth infections may contribute to a greener world.

The dynamic trophic architecture of open-ocean protist communities revealed through machine-guided metatranscriptomics.

Intricate networks of single-celled eukaryotes (protists) dominate carbon flow in the ocean. Their growth, demise, and interactions with other microorganisms drive the fluxes of biogeochemical elements through marine ecosystems. Mixotrophic protists are capable of both photosynthesis and ingestion of prey and are dominant components of open-ocean planktonic communities. Yet the role of mixotrophs in elemental cycling is obscured by their capacity to act as primary producers or heterotrophic consumers depending on factors that remain largely uncharacterized. Here, we develop and apply a machine learning model that predicts the in situ trophic mode of aquatic protists based on their patterns of gene expression. This approach leverages a public collection of protist transcriptomes as a training set to identify a subset of gene families whose transcriptional profiles predict trophic mode. We applied our model to nearly 100 metatranscriptomes obtained during two oceanographic cruises in the North Pacific and found community-level and population-specific evidence that abundant open-ocean mixotrophic populations shift their predominant mode of nutrient and carbon acquisition in response to natural gradients in nutrient supply and sea surface temperature. Metatranscriptomic data from ship-board incubation experiments revealed that abundant mixotrophic prymnesiophytes from the oligotrophic North Pacific subtropical gyre rapidly remodeled their transcriptome to enhance photosynthesis when supplied with limiting nutrients. Coupling this approach with experiments designed to reveal the mechanisms driving mixotroph physiology provides an avenue toward understanding the ecology of mixotrophy in the natural environment.

Regime shifts, trends, and variability of lake productivity at a global scale.

Lakes are often described as sentinels of global change. Phenomena like lake eutrophication, algal blooms, or reorganization in community composition belong to the most studied ecosystem regime shifts. However, although regime shifts have been well documented in several lakes, a global assessment of the prevalence of regime shifts is still missing, and, more in general, of the factors altering stability in lake status, is missing. Here, we provide a first global assessment of regime shifts and stability in the productivity of 1,015 lakes worldwide using trophic state index (TSI) time series derived from satellite imagery. We find that 12.8% of the lakes studied show regime shifts whose signatures are compatible with tipping points, while the number of detected regime shifts from low to high TSI has increased over time. Although our results suggest an overall stable picture for global lake dynamics, the limited instability signatures do not mean that lakes are insensitive to global change. Modeling the interaction between lake climatic, geophysical, and socioeconomic features and their stability properties, we find that the probability of a lake experiencing a tipping point increases with human population density in its catchment, while it decreases as the gross domestic product of that population increases. Our results show how quantifying lake productivity dynamics at a global scale highlights socioeconomic inequalities in conserving natural environments.

The interaction between warming and enrichment accelerates food-web simplification in freshwater systems.

Nutrient enrichment and climate warming threaten freshwater systems. Metabolic theory and the paradox of enrichment predict that both stressors independently can lead to simpler food-webs having fewer nodes, shorter food-chains and lower connectance, but cancel each other's effects when simultaneously present. Yet, these theoretical predictions remain untested in complex natural systems. We inferred the food-web structure of 256 lakes and 373 streams from standardized fish community samplings in France. Contrary to theoretical predictions, we found that warming shortens fish food-chain length and that this effect was magnified in enriched streams and lakes. Additionally, lakes experiencing enrichment exhibit lower connectance in their fish food-webs. Our study suggests that warming and enrichment interact to magnify food-web simplification in nature, raising further concerns about the fate of freshwater systems as climate change effects will dramatically increase in the coming decades.

Aspen recovery in northern Yellowstone: A comment on Brice et al. (2021).

Aspen sapling recruitment increased as browsing by elk decreased, following the 1995-96 reintroduction of wolves in Yellowstone National Park. We address claims by Brice et al. (2021) that previous studies exaggerated recent aspen recovery. We conclude that their results actually supported previous work showing a trophic cascade benefiting aspen.

The reorganization of predator-prey networks over 20 million years explains extinction patterns of mammalian carnivores.

Linking the species interactions occurring at the scale of local communities to their potential impact at evolutionary timescales is challenging. Here, we used the high-resolution fossil record of mammals from the Iberian Peninsula to reconstruct a timeseries of trophic networks spanning more than 20 million years and asked whether predator-prey interactions affected regional extinction patterns. We found that, despite small changes in species richness, trophic networks showed long-term trends, gradually losing interactions and becoming sparser towards the present. This restructuring of the ecological networks was driven by the loss of medium-sized herbivores, which reduced prey availability for predators. The decrease in prey availability was associated with predator longevity, such that predators with less available prey had greater extinction risk. These results not only reveal long-term trends in network structure but suggest that prey species richness in ecological communities may shape large scale patterns of extinction and persistence among predators.

Non-random sampling measures the occurrence but not the strength of a textbook trophic cascade.

Although sampling the five tallest young aspen in a stand is useful for detecting the occurrence of any aspen recruitment, this technique overestimates the population response of aspen to wolf reintroduction. Our original conclusion that random sampling described a trophic cascade that was weaker than the one described by non-random sampling is unchanged.

Population links between an insectivorous bird and moths disentangled through national-scale monitoring data.

Insects are key components of food chains, and monitoring data provides new opportunities to identify trophic relationships at broad spatial and temporal scales. Here, combining two monitoring datasets from Great Britain, we reveal how the population dynamics of the blue tit Cyanistes caeruleus are influenced by the abundance of moths - a core component of their breeding diet. We find that years with increased population growth for blue tits correlate strongly with high moth abundance, but population growth in moths and birds is less well correlated; suggesting moth abundance directly affects bird population change. Next, we identify moths that are important components of blue tit diet, recovering associations to species previously identified as key food sources such as the winter moth Operoptera brumata. Our work provides new evidence that insect abundance impacts bird population dynamics in natural communities and provides insight into spatial diet turnover at a national-scale.

Body size and trophic position determine the outcomes of species invasions along temperature and productivity gradients.

Species invasions are predicted to increase in frequency with global change, but quantitative predictions of how environmental filters and species traits influence the success and consequences of invasions for local communities are lacking. Here we investigate how invaders alter the structure, diversity and stability regime of simple communities across environmental gradients (habitat productivity, temperature) and community size structure. We simulate all three-species trophic modules (apparent and exploitative competition, trophic chain and intraguild predation). We predict that invasions most often succeed in warm and productive habitats and that successful invaders include smaller competitors, intraguild predators and comparatively small top predators. This suggests that species invasions and global change may facilitate the downsizing of food webs. Furthermore, we show that successful invasions leading to species substitutions rarely alter system stability, while invasions leading to increased diversity can destabilize or stabilize community dynamics depending on the environmental conditions and invader's trophic position.

Predator-driven behavioural shifts in a common lizard shape resource-flow from marine to terrestrial ecosystems.

Foraging decisions shape the structure of food webs. Therefore, a behavioural shift in a single species can potentially modify resource-flow dynamics of entire ecosystems. To examine this, we conducted a field experiment to assess foraging niche dynamics of semi-arboreal brown anole lizards in the presence/absence of predatory ground-dwelling curly-tailed lizards in a replicated set of island ecosystems. One year after experimental translocation, brown anoles exposed to these predators had drastically increased perch height and reduced consumption of marine-derived food resources. This foraging niche shift altered marine-to-terrestrial resource-flow dynamics and persisted in the diets of the first-generation offspring. Furthermore, female lizards that displayed more risk-taking behaviours consumed more marine prey on islands with predators present. Our results show how predator-driven rapid behavioural shifts can alter food-web connectivity between oceanic and terrestrial ecosystems and underscore the importance of studying behaviour-mediated niche shifts to understand ecosystem functioning in rapidly changing environments.

Food web context modifies predator foraging and weakens trophic interaction strength.

Trophic interaction modifications (TIM) are widespread in natural systems and occur when a third species indirectly alters the strength of a trophic interaction. Past studies have focused on documenting the existence and magnitude of TIMs; however, the underlying processes and long-term consequences remain elusive. To address this gap, we experimentally quantified the density-dependent effect of a third species on a predator's functional response. We conducted short-term experiments with ciliate communities composed of a predator, prey and non-consumable 'modifier' species. In both communities, increasing modifier density weakened the trophic interaction strength, due to a negative effect on the predator's space clearance rate. Simulated long-term dynamics indicate quantitative differences between models that account for TIMs or include only pairwise interactions. Our study demonstrates that TIMs are important to understand and predict community dynamics and highlights the need to move beyond focal species pairs to understand the consequences of species interactions in communities.