Complexity Thoughts: Issue #51
Unraveling complexity: building knowledge, one paper at a time
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From the lab
Distorted insights from human mobility data
Assuming that your single human mobility data set (i.e., a network of human flows between two spatial areas) is representative of universal behavior might be a weaker assumption than previously thought… Here, we show that not only this assumption does not hold across distinct data sets, but it can lead to wrong results when coupling that dynamics with other processes, such as epidemic spreading.
The description of human mobility is at the core of many fundamental applications ranging from urbanism and transportation to epidemics containment. Data about human movements, once scarce, is now widely available thanks to new sources such as phone call detail records, GPS devices, or Smartphone apps. Nevertheless, it is still common to rely on a single dataset by implicitly assuming that the statistical properties observed are robust regardless of data gathering and processing techniques. Here, we test this assumption on a broad scale by comparing human mobility datasets obtained from 7 different data-sources, tracing 500+ millions individuals in 145 countries. We report wide quantifiable differences in the resulting mobility networks and in the displacement distribution. These variations impact processes taking place on these networks like epidemic spreading. Our results point to the need for disclosing the data processing and, overall, to follow good practices to ensure robust and reproducible results.
Evolution
The Angiosperm Terrestrial Revolution buffered ants against extinction
All lineages have experienced changes in their diversity dynamics, sometimes leading to their complete disappearance from Earth. The underlying causes of these extinctions or diversifications often remain puzzling, particularly when delving into deep time. Using an unprecedented combination of paleontological and neontological data, we investigate the past diversity dynamics of stem and crown ants. Our results challenge one of the most common hypotheses explaining ant extinction: the competitive exclusion of stem ants by crown ants. Instead, the Angiosperm Terrestrial Revolution acted as a buffer against extinction and a driver of diversification in ants. Our approach clarifies one of the most widely accepted patterns in insect–plant diversification.
With ~14,000 extant species, ants are ubiquitous and of tremendous ecological importance. They have undergone remarkable diversification throughout their evolutionary history. However, the drivers of their diversity dynamics are not well quantified or understood. Previous phylogenetic analyses have suggested patterns of diversity dynamics associated with the Angiosperm Terrestrial Revolution (ATR), but these studies have overlooked valuable information from the fossil record. To address this gap, we conducted a comprehensive analysis using a large dataset that includes both the ant fossil record (~24,000 individual occurrences) and neontological data (~14,000 occurrences), and tested four hypotheses proposed for ant diversification: co-diversification, competitive extinction, hyper-specialization, and buffered extinction. Taking into account biases in the fossil record, we found three distinct diversification periods (the latest Cretaceous, Eocene, and Oligo-Miocene) and one extinction period (Late Cretaceous). The competitive extinction hypothesis between stem and crown ants is not supported. Instead, we found support for the co-diversification, buffered extinction, and hyper-specialization hypotheses. The environmental changes of the ATR, mediated by the angiosperm radiation, likely played a critical role in buffering ants against extinction and favoring their diversification by providing new ecological niches, such as forest litter and arboreal nesting sites, and additional resources. We also hypothesize that the decline and extinction of stem ants during the Late Cretaceous was due to their hyper-specialized morphology, which limited their ability to expand their dietary niche in changing environments. This study highlights the importance of a holistic approach when studying the interplay between past environments and the evolutionary trajectories of organisms.
Ecosystems
Gut microbiome strain-sharing within isolated village social networks
It was not easy to “classify” this paper, since it connects concepts from biology and human behavior. Eventually, I have opted for ecosystem.
When humans assemble into face-to-face social networks, they create an extended social environment that permits exposure to the microbiome of others, thereby shaping the composition and diversity of the microbiome at individual and population levels1,2,3,4,5,6. Here we use comprehensive social network mapping and detailed microbiome sequencing data in 1,787 adults within 18 isolated villages in Honduras7 to investigate the relationship between network structure and gut microbiome composition. Using both species-level and strain-level data, we show that microbial sharing occurs between many relationship types, notably including non-familial and non-household connections. Furthermore, strain-sharing extends to second-degree social connections, suggesting the relevance of a person’s broader network. We also observe that socially central people are more microbially similar to the overall village than socially peripheral people. Among 301 people whose microbiome was re-measured 2 years later, we observe greater convergence in strain-sharing in connected versus otherwise similar unconnected co-villagers. Clusters of species and strains occur within clusters of people in village social networks, meaning that social networks provide the social niches within which microbiome biology and phenotypic impact are manifested.
Across many ecosystems, declining biodiversity leads to lower biomass and loss of other ecosystem functions. Much of the research in this area has focused on plant communities, with less attention paid to consumers, who play the important role of accumulating and synthesizing organic nutrients. Shipley et al. investigated how the diversity of insects and spiders affects community-level concentrations of polyunsaturated fatty acids (PUFAs), one type of essential nutrient. They found higher biomass and higher PUFA mass in more diverse communities in both terrestrial and aquatic systems and in different land uses. In human-dominated systems, both predator biomass and PUFA biomass were lower at a given level of species richness than in natural systems, suggesting a negative shift in function. —Bianca Lopez
Human land-use intensification threatens arthropod (for example, insect and spider) biodiversity across aquatic and terrestrial ecosystems. Insects and spiders play critical roles in ecosystems by accumulating and synthesizing organic nutrients such as polyunsaturated fatty acids (PUFAs). However, links between biodiversity and nutrient content of insect and spider communities have yet to be quantified. We relate insect and spider richness to biomass and PUFA-mass from stream and terrestrial communities encompassing nine land uses. PUFA-mass and biomass relate positively to biodiversity across ecosystems. In terrestrial systems, human-dominated areas have lower biomass and PUFA-mass than more natural areas, even at equivalent levels of richness. Aquatic ecosystems have consistently higher PUFA-mass than terrestrial ecosystems. Our findings reinforce the importance of conserving biodiversity and highlight the distinctive benefits of aquatic biodiversity.
Biological Systems
The disciplinary matrix of holobiont biology
The importance of microbiomes in host biology guides an intriguing convergence of micro- and macrobiological worlds. Consequently, the multidisciplinary framework of holobiont biology has emerged to integrate modes of genomic and functional variation that emphasize the centrality of microorganisms to the biosphere and the science of microbiome- based solutions for wide-ranging host activities, spanning agricultural production, conservation biology, and human diseases (1). The terms holobiont (the collection of host and associated microbial cells) and hologenome (all multispecies genetic material in the holobiont) are important to this conceptual change because they unify microbial symbiosis into the structure, function, and evolution of macroorganisms (2). Host organisms are thus defined to contain other organisms—viruses, bacteria, protozoa, and fungi—and their genomes. The functional relevance of these host-microbe associations will vary from inconsequential to harmful or essential, depending on the interactive milieu of members in the holobiont system (3).
Soil microbiomes show consistent and predictable responses to extreme events
Increasing extreme climatic events threaten the functioning of terrestrial ecosystems1,2. Because soil microbes govern key biogeochemical processes, understanding their response to climate extremes is crucial in predicting the consequences for ecosystem functioning3,4. Here we subjected soils from 30 grasslands across Europe to four contrasting extreme climatic events under common controlled conditions (drought, flood, freezing and heat), and compared the response of soil microbial communities and their functioning with those of undisturbed soils. Soil microbiomes exhibited a small, but highly consistent and phylogenetically conserved, response under the imposed extreme events. Heat treatment most strongly impacted soil microbiomes, enhancing dormancy and sporulation genes and decreasing metabolic versatility. Microbiome response to heat in particular could be predicted by local climatic conditions and soil properties, with soils that do not normally experience the extreme conditions being imposed being most vulnerable. Our results suggest that soil microbiomes from different climates share unified responses to extreme climatic events, but that predicting the extent of community change may require knowledge of the local microbiome. These findings advance our understanding of soil microbial responses to extreme events, and provide a first step for making general predictions about the impact of extreme climatic events on soil functioning.
Neuroscience
An energy costly architecture of neuromodulators for human brain evolution and cognition
In comparison to other species, the human brain exhibits one of the highest energy demands relative to body metabolism. It remains unclear whether this heightened energy demand uniformly supports an enlarged brain or if specific signaling mechanisms necessitate greater energy. We hypothesized that the regional distribution of energy demands will reveal signaling strategies that have contributed to human cognitive development. We measured the energy distribution within the brain functional connectome using multimodal brain imaging and found that signaling pathways in evolutionarily expanded regions have up to 67% higher energetic costs than those in sensory-motor regions. Additionally, histology, transcriptomic data, and molecular imaging independently reveal an up-regulation of signaling at G-protein-coupled receptors in energy-demanding regions. Our findings indicate that neuromodulator activity is predominantly involved in cognitive functions, such as reading or memory processing. This study suggests that an up-regulation of neuromodulator activity, alongside increased brain size, is a crucial aspect of human brain evolution.
Neuronal sequences in population bursts encode information in human cortex
Neurons in the human anterior temporal lobe fire in precise sequences during visual tasks, while encoding rich information about both categories and individual exemplars. This paper reports a discovery that reveals a complementary coding mechanism to traditional spike rates, highlighting the critical role of temporal order in neural communication to processing visual stimuli. See also this research briefing.
Neural coding has traditionally been examined through changes in firing rates and latencies in response to different stimuli1,2,3,4,5. However, populations of neurons can also exhibit transient bursts of spiking activity, wherein neurons fire in a specific temporal order or sequence6,7,8. The human brain may utilize these neuronal sequences within population bursts to efficiently represent information9,10,11,12, thereby complementing the well-known neural code based on spike rate or latency. Here we examined this possibility by recording the spiking activity of populations of single units in the human anterior temporal lobe as eight participants performed a visual categorization task. We find that population spiking activity organizes into bursts during the task. The temporal order of spiking across the activated units within each burst varies across stimulus categories, creating unique stereotypical sequences for individual categories as well as for individual exemplars within a category. The information conveyed by the temporal order of spiking activity is separable from and complements the information conveyed by the units’ spike rates or latencies following stimulus onset. Collectively, our data provide evidence that the human brain contains a complementary code based on the neuronal sequence within bursts of population spiking to represent information.
Human behavior
See From the Lab above.
Origin of life
Prebiotic chiral transfer from self-aminoacylating ribozymes may favor either handedness
Modern life is essentially homochiral, containing D-sugars in nucleic acid backbones and L-amino acids in proteins. Since coded proteins are theorized to have developed from a prebiotic RNA World, the homochirality of L-amino acids observed in all known life presumably resulted from chiral transfer from a homochiral D-RNA World. This transfer would have been mediated by aminoacyl-RNAs defining the genetic code. Previous work on aminoacyl transfer using tRNA mimics has suggested that aminoacylation using D-RNA may be inherently biased toward reactivity with L-amino acids, implying a deterministic path from a D-RNA World to L-proteins. Using a model system of self-aminoacylating D-ribozymes and epimerizable activated amino acid analogs, we test the chiral selectivity of 15 ribozymes derived from an exhaustive search of sequence space. All of the ribozymes exhibit detectable selectivity, and a substantial fraction react preferentially to produce the D-enantiomer of the product. Furthermore, chiral preference is conserved within sequence families. These results are consistent with the transfer of chiral information from RNA to proteins but do not support an intrinsic bias of D-RNA for L-amino acids. Different aminoacylation structures result in different directions of chiral selectivity, such that L-proteins need not emerge from a D-RNA World.
Symmetry breaking and chiral amplification in prebiotic ligation reactions
The single chirality of biological molecules is a signature of life. Yet, rationalizing how single chirality emerged remains a challenging goal1. Research has commonly focused on initial symmetry breaking and subsequent enantioenrichment of monomer building blocks—sugars and amino acids—that compose the genetic polymers RNA and DNA as well as peptides. If these building blocks are only partially enantioenriched, however, stalling of chain growth may occur, whimsically termed in the case of nucleic acids as “the problem of original syn”2. Here, in studying a new prebiotically plausible route to proteinogenic peptides3,4,5, we discovered that the reaction favours heterochiral ligation (that is, the ligation of l monomers with d monomers). Although this finding seems problematic for the prebiotic emergence of homochiral l-peptides, we demonstrate, paradoxically, that this heterochiral preference provides a mechanism for enantioenrichment in homochiral chains. Symmetry breaking, chiral amplification and chirality transfer processes occur for all reactants and products in multicomponent competitive reactions even when only one of the molecules in the complex mixture exhibits an imbalance in enantiomer concentrations (non-racemic). Solubility considerations rationalize further chemical purification and enhanced chiral amplification. Experimental data and kinetic modelling support this prebiotically plausible mechanism for the emergence of homochiral biological polymers.
Reconstructing the last common ancestor of all eukaryotes
Understanding the origin of eukaryotic cells is one of the most difficult problems in all of biology. A key challenge relevant to the question of eukaryogenesis is reconstructing the gene repertoire of the last eukaryotic common ancestor (LECA). As data sets grow, sketching an accurate genomics-informed picture of early eukaryotic cellular complexity requires provision of analytical resources and a commitment to data sharing. Here, we summarise progress towards understanding the biology of LECA and outline a community approach to inferring its wider gene repertoire. Once assembled, a robust LECA gene set will be a useful tool for evaluating alternative hypotheses about the origin of eukaryotes and understanding the evolution of traits in all descendant lineages, with relevance in diverse fields such as cell biology, microbial ecology, biotechnology, agriculture, and medicine. In this Consensus View, we put forth the status quo and an agreed path forward to reconstruct LECA’s gene content.