Organ Evolution: Emergence of Multicellular Function.

Instances of multicellularity across the tree of life have fostered the evolution of complex organs composed of distinct cell types that cooperate, producing emergent biological functions. How organs originate is a fundamental evolutionary problem that has eluded deep mechanistic and conceptual understanding. Here I propose a cell- to organ-level transitions framework, whereby cooperative division of labor originates and becomes entrenched between cell types through a process of functional niche creation, cell-type subfunctionalization, and irreversible ratcheting of cell interdependencies. Comprehending this transition hinges on explaining how these processes unfold molecularly in evolving populations. Recent single-cell transcriptomic studies and analyses of terminal fate specification indicate that cellular functions are conferred by modular gene expression programs. These discrete components of functional variation may be deployed or combined within cells to introduce new properties into multicellular niches, or partitioned across cells to establish division of labor. Tracing gene expression program evolution at the level of single cells in populations may reveal transitions toward organ complexity.

The Budding Neuroscience of Ant Social Behavior.

Ant physiology has been fashioned by 100 million years of social evolution. Ants perform many sophisticated social and collective behaviors yet possess nervous systems similar in schematic and scale to that of the fruit fly Drosophila melanogaster, a popular solitary model organism. Ants are thus attractive complementary subjects to investigate adaptations pertaining to complex social behaviors that are absent in flies. Despite research interest in ant behavior and the neurobiological foundations of sociality more broadly, our understanding of the ant nervous system is incomplete. Recent technical advances have enabled cutting-edge investigations of the nervous system in a fashion that is less dependent on model choice, opening the door for mechanistic social insect neuroscience. In this review, we revisit important aspects of what is known about the ant nervous system and behavior, and we look forward to how functional circuit neuroscience in ants will help us understand what distinguishes solitary animals from highly social ones.

The physical soldier caste of an invasive, human-infecting flatworm is morphologically extreme and obligately sterile.

We show that the globally invasive, human-infectious flatworm, Haplorchis pumilio, possesses the most physically specialized soldier caste yet documented in trematodes. Soldiers occur in colonies infecting the first intermediate host, the freshwater snail Melanoides tuberculata, and are readily distinguishable from immature and mature reproductive worms. Soldiers possess a pharynx five times absolutely larger than those of immature and mature reproductives, lack a germinal mass, and have a different developmental trajectory than reproductives, indicating that H. pumilio soldiers constitute a reproductively sterile physical caste. Neither immature nor mature reproductives showed aggression in in vitro trials, but soldiers readily attacked heterospecific trematodes that coinfect their host. Ecologically, we calculate that H. pumilio caused ~94% of the competitive deaths in the guild of trematodes infecting its host snail in its invasive range in southern California. Despite being a dominant competitor, H. pumilio soldiers did not attack conspecifics from other colonies. All prior reports documenting division of labor and a trematode soldier caste have involved soldiers that may be able to metamorphose to the reproductive stage and have been from nonhuman-infectious marine species; this study provides clear evidence for an obligately sterile trematode soldier, while extending the phenomenon of a trematode soldier caste to freshwater and to an invasive species of global public health concern.

Genetics and Evolution of Social Behavior in Insects.

The study of insect social behavior has offered tremendous insight into the molecular mechanisms mediating behavioral and phenotypic plasticity. Genomic applications to the study of eusocial insect species, in particular, have led to several hypotheses for the processes underlying the molecular evolution of behavior. Advances in understanding the genetic control of social organization have also been made, suggesting an important role for supergenes in the evolution of divergent behavioral phenotypes. Intensive study of social phenotypes across species has revealed that behavior and caste are controlled by an interaction between genetic and environmentally mediated effects and, further, that gene expression and regulation mediate plastic responses to environmental signals. However, several key methodological flaws that are hindering progress in the study of insect social behavior remain. After reviewing the current state of knowledge, we outline ongoing challenges in experimental design that remain to be overcome in order to advance the field.

Behavioral genetics and genomics: Mendel's peas, mice, and bees.

The question of the heritability of behavior has been of long fascination to scientists and the broader public. It is now widely accepted that most behavioral variation has a genetic component, although the degree of genetic influence differs widely across behaviors. Starting with Mendel's remarkable discovery of "inheritance factors," it has become increasingly clear that specific genetic variants that influence behavior can be identified. This goal is not without its challenges: Unlike pea morphology, most natural behavioral variation has a complex genetic architecture. However, we can now apply powerful genome-wide approaches to connect variation in DNA to variation in behavior as well as analyses of behaviorally related variation in brain gene expression, which together have provided insights into both the genetic mechanisms underlying behavior and the dynamic relationship between genes and behavior, respectively, in a wide range of species and for a diversity of behaviors. Here, we focus on two systems to illustrate both of these approaches: the genetic basis of burrowing in deer mice and transcriptomic analyses of division of labor in honey bees. Finally, we discuss the troubled relationship between the field of behavioral genetics and eugenics, which reminds us that we must be cautious about how we discuss and contextualize the connections between genes and behavior, especially in humans.

When being flexible matters: Ecological underpinnings for the evolution of collective flexibility and task allocation.

Task allocation is a central feature of collective organization. Living collective systems, such as multicellular organisms or social insect colonies, have evolved diverse ways to allocate individuals to different tasks, ranging from rigid, inflexible task allocation that is not adjusted to changing circumstances to more fluid, flexible task allocation that is rapidly adjusted to the external environment. While the mechanisms underlying task allocation have been intensely studied, it remains poorly understood whether differences in the flexibility of task allocation can be viewed as adaptive responses to different ecological contexts­for example, different degrees of temporal variability. Motivated by this question, we develop an analytically tractable mathematical framework to explore the evolution of task allocation in dynamic environments. We find that collective flexibility is not necessarily always adaptive, and fails to evolve in environments that change too slowly (relative to how long tasks can be left unattended) or too quickly (relative to how rapidly task allocation can be adjusted). We further employ the framework to investigate how environmental variability impacts the internal organization of task allocation, which allows us to propose adaptive explanations for some puzzling empirical observations, such as seemingly unnecessary task switching under constant environmental conditions, apparent task specialization without efficiency benefits, and high levels of individual inactivity. Altogether, this work provides a general framework for probing the evolved diversity of task allocation strategies in nature and reinforces the idea that considering a system's ecology is crucial to explaining its collective organization.

Neural mechanisms distinguishing two types of cooperative problem-solving approaches: An fNIRS hyperscanning study.

Collaborative cooperation (CC) and division of labor cooperation (DLC) are two prevalent forms of cooperative problem-solving approaches in daily life. Despite extensive research on the neural mechanisms underlying cooperative problem-solving approaches, a notable gap exists between the neural processes that support CC and DLC. The present study utilized a functional near-infrared spectroscopy (fNIRS) hyperscanning technique along with a classic cooperative tangram puzzle task to investigate the neural mechanisms engaged by both friends and stranger dyads during CC versus DLC. The key findings of this study were as follows: (1) Dyads exhibited superior behavioral performance in the DLC task than in the CC task. The CC task bolstered intra-brain functional connectivity and inter-brain synchrony (IBS) in regions linked to the mirror neuron system (MNS), spatial perception (SP) and cognitive control. (2) Friend dyads showed stronger IBS in brain regions associated with the MNS than stranger dyads. (3) Perspective-taking predicted not only dyads' behavioral performance in the CC task but also their IBS in brain regions associated with SP during the DLC task. Taken together, these findings elucidate the divergent behavioral performance and neural connection patterns between the two cooperative problem-solving approaches. This study provides novel insights into the various neurocognitive processes underlying flexible coordination strategies in real-world cooperative contexts.

Engineering carbon source division of labor for efficient α-carotene production in Corynebacterium glutamicum.

Effective utilization of glucose, xylose, and acetate, common carbon sources in lignocellulose hydrolysate, can boost biomanufacturing economics. However, carbon leaks into biomass biosynthesis pathways instead of the intended target product remain to be optimized. This study aimed to enhance α-carotene production by optimizing glucose, xylose, and acetate utilization in a high-efficiency Corynebacterium glutamicum cell factory. Heterologous xylose pathway expression in C. glutamicum resulted in strain m4, exhibiting a two-fold increase in α-carotene production from xylose compared to glucose. Xylose utilization was found to boost the biosynthesis of pyruvate and acetyl-CoA, essential precursors for carotenoid biosynthesis. Additionally, metabolic engineering including pck, pyc, ppc, and aceE deletion, completely disrupted the metabolic connection between glycolysis and the TCA cycle, further enhancing α-carotene production. This strategic intervention directed glucose and xylose primarily towards target chemical production, while acetate supplied essential metabolites for cell growth recovery. The engineered strain C. glutamicum m8 achieved 30 mg/g α-carotene, 67% higher than strain m4. In fed-batch fermentation, strain m8 produced 1802 mg/L of α-carotene, marking the highest titer reported to date in microbial fermentation. Moreover, it exhibited excellent performance in authentic lignocellulosic hydrolysate, producing 216 mg/L α-carotene, 1.45 times higher than the initial strain (m4). These labor-division strategies significantly contribute to the development of clean processes for producing various valuable chemicals from lignocellulosic resources.

Evolution of genome fragility enables microbial division of labor.

Division of labor can evolve when social groups benefit from the functional specialization of its members. Recently, a novel means of coordinating the division of labor was found in the antibiotic-producing bacterium Streptomyces coelicolor, where specialized cells are generated through large-scale genomic re-organization. We investigate how the evolution of a genome architecture enables such mutation-driven division of labor, using a multiscale computational model of bacterial evolution. In this model, bacterial behavior-antibiotic production or replication-is determined by the structure and composition of their genome, which encodes antibiotics, growth-promoting genes, and fragile genomic loci that can induce chromosomal deletions. We find that a genomic organization evolves, which partitions growth-promoting genes and antibiotic-coding genes into distinct parts of the genome, separated by fragile genomic loci. Mutations caused by these fragile sites mostly delete growth-promoting genes, generating sterile, and antibiotic-producing mutants from weakly-producing progenitors, in agreement with experimental observations. This division of labor enhances the competition between colonies by promoting antibiotic diversity. These results show that genomic organization can co-evolve with genomic instabilities to enable reproductive division of labor.

Foraging task specialization in honey bees (Apis mellifera): the contribution of floral rewards to the learning performance of pollen and nectar foragers.

Social insects live in communities where cooperative actions heavily rely on the individual cognitive abilities of their members. In the honey bee (Apis mellifera), the specialization in nectar or pollen collection is associated with variations in gustatory sensitivity, affecting both associative and non-associative learning. Gustatory sensitivity fluctuates as a function of changes in motivation for the specific floral resource throughout the foraging cycle, yet differences in learning between nectar and pollen foragers at the onset of food collection remain unexplored. Here, we examined nectar and pollen foragers captured upon arrival at food sources. We subjected them to an olfactory proboscis extension reflex (PER) conditioning using a 10% sucrose solution paired (S10%+P) or unpaired (S10%) with pollen as a co-reinforcement. For non-associative learning, we habituated foragers with S10%+P or S10%, followed by dishabituation tests with either a 50% sucrose solution paired (S50%+P) or unpaired (S50%) with pollen. Our results indicate that pollen foragers show lower performance than nectar foragers when conditioned with S10%. Interestingly, performance improves to levels similar to those of nectar foragers when pollen is included as a rewarding stimulus (S10%+P). In non-associative learning, pollen foragers tested with S10%+P displayed a lower degree of habituation than nectar foragers and a higher degree of dishabituation when pollen was used as the dishabituating stimulus (S10%+P). Altogether, our results support the idea that pollen and nectar honey bee foragers differ in their responsiveness to rewards, leading to inter-individual differences in learning that contribute to foraging specialization.

Negotiating Work and Family Spheres: The Dyadic Effects of Flexible Work Arrangements on Fertility Among Dual-Earner Heterosexual Couples.

Academics and policymakers have suggested making flexible work arrangements (FWAs) the default in workplaces to promote a family-friendly workplace culture conducive to having and raising children. However, systematic research investigating how FWAs, as a long-term approach to negotiating work-family spheres, are related to fertility among dual-earner heterosexual couples is limited. Drawing on the linked-lives perspective, we theorize the relationship between FWAs and fertility among couples and potential variation depending on the interplay of both spouses' work and family characteristics. We test our hypotheses using longitudinal couple-level dyadic data in the United Kingdom (2010-2022). We find that although FWA availability alone is unrelated to fertility, wives' (not husbands') FWA use is significantly associated with a higher probability of experiencing a first birth. Moreover, the effect of wives' FWA use is particularly pronounced when both spouses work in professional and managerial occupations and when husbands contribute a larger proportion of income and at least equal housework. This study reveals a gendered effect of FWAs on fertility across work-family arrangements, deepening our understanding of couple-level dynamics in the fertility process.

Doing Genders: Partner's Gender and Labor Market Behavior.

Partnered men and women show consistently gendered patterns of labor market behavior. We test whether not only a person's own gender, but also their partner's gender shapes hours worked. We use Dutch administrative population data on almost 5,000 persons who had both male and female partners, whose hours worked we observe monthly over 15 years. We argue that this provides a unique setting to assess the relevance of partner's gender for labor market behavior. Using two-way fixed effects and fixed-effects individual slopes models, we find that both men and women tend to work more hours when partnered with a female partner compared to a male partner. These results align with our hypothesis that a partner's gender influences labor market behavior. For women, we conclude that this finding may be (partly) explained by marital and motherhood status. Additionally, we discovered that women decrease their hours worked to a lesser extent when caring for a child if they have a female partner. Finally, we found that for men, the positive association between own and partner's hours worked is weaker when one has a female partner, indicating a higher degree of specialization within these couples.

Microbial redox cycling enhances ecosystem thermodynamic efficiency and productivity.

Microbial life in low-energy ecosystems relies on individual energy conservation, optimizing energy use in response to interspecific competition and mutualistic interspecific syntrophy. Our study proposes a novel community-level strategy for increasing energy use efficiency. By utilizing an oxidation-reduction (redox) reaction network model that represents microbial redox metabolic interactions, we investigated multiple species-level competition and cooperation within the network. Our results suggest that microbial functional diversity allows for metabolic handoffs, which in turn leads to increased energy use efficiency. Furthermore, the mutualistic division of labour and the resulting complexity of redox pathways actively drive material cycling, further promoting energy exploitation. Our findings reveal the potential of self-organized ecological interactions to develop efficient energy utilization strategies, with important implications for microbial ecosystem functioning and the co-evolution of life and Earth.

Evolution and functionalization of vitellogenin genes in the termite Reticulitermes speratus.

Eusociality has been commonly observed in distinct animal lineages. The reproductive division of labor is a particular feature, achieved by the coordination between fertile and sterile castes within the same nest. The sociogenomic approach in social hymenopteran insects indicates that vitellogenin (Vg) has undergone neo-functionalization in sterile castes. Here, to know whether Vgs have distinct roles in nonreproductive castes in termites, we investigated the unique characteristics of Vgs in the rhinotermitid termite Reticulitermes speratus. The four Vgs were identified from R. speratus (RsVg1-4), and RsVg3 sequences were newly identified using the RACE method. Molecular phylogenetic analysis supported the monophyly of the four termite Vgs. Moreover, the termites Vg1-3 and Vg4 were positioned in two different clades. The  dN/dS ratios indicated that the branch leading to the common ancestor of termite Vg4 was under weak purifying selection. Expression analyses among castes (reproductives, workers, and soldiers) and females (nymphs, winged alates, and queens) showed that RsVg1-3 was highly expressed in fertile queens. In contrast, RsVg4 was highly expressed in workers and female nonreproductives (nymphs and winged adults). Localization of RsVg4 messenger RNA was confirmed in the fat body of worker heads and abdomens. These results suggest that Vg genes are functionalized after gene duplication during termite eusocial transition and that Vg4 is involved in nonreproductive roles in termites.

Mediation of Bacterial Interactions via a Novel Membrane-Based Segregator to Enhance Biological Nitrogen Removal.

The regulation of microbial subpopulations in wastewater treatment plants (WWTPs) with desired functions can guarantee nutrient removal. In nature, "good fences make good neighbors," which can be applied to engineering microbial consortia. Herein, a membrane-based segregator (MBSR) was proposed, where porous membranes not only promote the diffusion of metabolic products but also isolate incompatible microbes. The MBSR was integrated with an anoxic/aerobic membrane bioreactor (i.e., an experimental MBR). The long-term operation showed that the experimental MBR exhibited higher nitrogen removal (10.45 ± 2.73 mg/L total nitrogen) than the control MBR (21.68 ± 4.23 mg/L) in the effluent. The MBSR resulted in much lower oxygen reduction potential in the anoxic tank of the experimental MBR (-82.00 mV) compared to that of the control MBR (83.25 mV). The lower oxygen reduction potential can inevitably aid in the occurrence of denitrification. The 16S rRNA sequencing showed that the MBSR significantly enriched acidogenic consortia, which yielded considerable volatile fatty acids by fermenting the added carbon sources and allowed efficient transfer of these small molecules to the denitrifying community. Moreover, the sludge communities of the experimental MBR harbored a higher abundance of denitrifying bacteria than those of the control MBR. Metagenomic analysis further corroborated these sequencing results. The spatially structured microbial communities in the experimental MBR system demonstrate the practicability of the MBSR, achieving nitrogen removal efficiency superior to that of mixed populations. Our study provides an engineering method for modulating the assembly and metabolic division of labor of subpopulations in WWTPs. IMPORTANCE This study provides an innovative and applicable method for regulating subpopulations (activated sludge and acidogenic consortia), which contributes to the precise control of the metabolic division of labor in biological wastewater treatment processes.

Plastic brain structure changes associated with the division of labor and aging in termites.

Division of labor is a prominent feature of social insect societies, where different castes engage in different specialized tasks. As brain differences are associated with behavioral differences, brain anatomy may be linked to caste polymorphism. Here, we show that termite brain morphology changes markedly with caste differentiation and age in the termite, Reticulitermes speratus. Brain morphology was shown to be associated with reproductive division of labor, with reproductive individuals (alates and neotenic reproductives) having larger brains than nonreproductives (workers and soldiers). Micro-computed tomography (CT) imaging and dissection observations showed that the king's brain morphology changed markedly with shrinkage of the optic lobes during their long life in the dark. Behavioral experiments showed that mature primary kings lose visual function as a result of optic lobe shrinkage. These results suggested that termites restructure their nervous systems to perform necessary tasks as they undergo caste differentiation, and that they also show flexible changes in brain morphology even after the final molt. This study showed that brain morphology in social insects is linked to caste and aging, and that the evolution of the division of labor is underpinned by the development of diverse neural systems for specialized tasks.

Human consumption of large herbivore digesta and its implications for foraging theory.

Vegetal matter undergoing digestion in herbivores' stomachs and intestines, digesta, can be an important source of dietary carbohydrates for human foragers. Digesta significantly increases large herbivores' total caloric yield and broadens their nutritional profile to include three key macronutrients (protein, fat, and carbohydrates) in amounts sufficient to sustain small foraging groups for multiple days without supplementation. Ethnographic reports of routine digesta consumption are limited to high latitudes, but the practice may have had a wider distribution prehistorically. Including this underappreciated resource in our foraging hypotheses and models can substantively change their predictions. Assessing the explanatory power of kilocalorie-centered models relative to ones that attend to humans' other nutritional requirements can help us better address major questions in evolutionary anthropology. This paper explores the foraging implications of digesta in two contexts-sex-divided subsistence labor and archaeologically observed increases in plant use and sedentism-using estimates of available protein and carbohydrates in the native tissues and digesta, respectively, of a large ruminant herbivore (Bison bison).

Gender Inequality Reinforced: The Impact of a Child's Health Shock on Parents' Labor Market Trajectories.

This article employs a couple-level framework to examine how a child's severe illness affects within-family gender inequality. We study parental labor market responses to a child's cancer diagnosis by exploiting an event-study methodology and rich individual-level administrative data on hospitalizations and labor market variables for the total population in Finland. We find that a child's cancer negatively affects the mother's and the father's labor income. The effect is considerably larger for women, increasing gender inequality beyond the well-documented motherhood penalty. We test three potential moderators explaining the more negative outcomes among mothers: (1) breadwinner status, (2) adherence to traditional gender roles and conservative values, and (3) the child's care needs. We find that mothers who are the main breadwinner experience a smaller reduction in their household income contribution than other mothers. Additionally, working in a gender-typical industry and a child's augmented care needs reinforce mothers' gendered responses. These findings contribute to the literature by providing new insights into gender roles when a child falls ill and demonstrating the effects of child health on gender inequality in two-parent households.

Who should see the patient? on deviations from preferred patient-provider assignments in hospitals.

In various organizations including hospitals, individuals are not forced to follow specific assignments, and thus, deviations from preferred task assignments are common. This is due to the conventional wisdom that professionals should be given the flexibility to deviate from preferred assignments as needed. It is unclear, however, whether and when this conventional wisdom is true. We use evidence on the assignments of generalist and specialists to patients in our partner hospital (a children's hospital), and generate insights into whether and when hospital administrators should disallow such flexibility. We do so by identifying 73 top medical diagnoses and using detailed patient-level electronic medical record (EMR) data of more than 4,700 hospitalizations. In parallel, we conduct a survey of medical experts and utilized it to identify the preferred provider type that should have been assigned to each patient. Using these two sources of data, we examine the consequence of deviations from preferred provider assignments on three sets of performance measures: operational efficiency (measured by length of stay), quality of care (measured by 30-day readmissions and adverse events), and cost (measured by total charges). We find that deviating from preferred assignments is beneficial for task types (patients' diagnosis in our setting) that are either (a) well-defined (improving operational efficiency and costs), or (b) require high contact (improving costs and adverse events, though at the expense of lower operational efficiency). For other task types (e.g., highly complex or resource-intensive tasks), we observe that deviations are either detrimental or yield no tangible benefits, and thus, hospitals should try to eliminate them (e.g., by developing and enforcing assignment guidelines). To understand the causal mechanism behind our results, we make use of mediation analysis and find that utilizing advanced imaging (e.g., MRIs, CT scans, or nuclear radiology) plays an important role in how deviations impact performance outcomes. Our findings also provide evidence for a "no free lunch" theorem: while for some task types, deviations are beneficial for certain performance outcomes, they can simultaneously degrade performance in terms of other dimensions. To provide clear recommendations for hospital administrators, we also consider counterfactual scenarios corresponding to imposing the preferred assignments fully or partially, and perform cost-effectiveness analyses. Our results indicate that enforcing the preferred assignments either for all tasks or only for resource-intensive tasks is cost-effective, with the latter being the superior policy. Finally, by comparing deviations during weekdays and weekends, early shifts and late shifts, and high congestion and low congestion periods, our results shed light on some environmental conditions under which deviations occur more in practice.

Meta-Analysis of Public RNA Sequencing Data Revealed Potential Key Genes Associated with Reproductive Division of Labor in Social Hymenoptera and Termites.

Eusociality in insects has evolved independently many times. One of the most notable characteristics of eusociality is the reproductive division of labor. In social insects, the reproductive division of labor is accomplished by queens and workers. Transcriptome analyses of queens and workers have been conducted for various eusocial species. However, the genes that regulate the reproductive division of labor across all or multiple eusocial species have not yet been fully elucidated. Therefore, we conducted a meta-analysis using publicly available RNA-sequencing data from four major groups of social insects. In this meta-analysis, we collected 258 pairs (queen vs. worker) of RNA-sequencing data from 34 eusocial species. The meta-analysis identified a total of 20 genes that were differentially expressed in queens or workers. Out of these, 12 genes have not previously been reported to be involved in the reproductive division of labor. Functional annotation of these 20 genes in other organisms revealed that they could be regulators of behaviors and physiological states related to the reproductive division of labor. These 20 genes, revealed using massive datasets of numerous eusocial insects, may be key regulators of the reproductive division of labor.