Ants have remarkably diverse diets and extraordinary species richness, making them an excellent model system to study the evolution of taste. In this entirely eusocial clade, food choice and the mechanisms that regulate feeding have both individual and social dimensions. How taste receptors and sensory processing drive food preferences to generate dietary breadth in ants is poorly understood. It is additionally unclear how elements of colony organization such as division of labor and social food flow impact the mechanistic basis and evolution of taste. Previous work on dipteran, lepidopteran, and hymenopteran gustatory systems, while foundational, provide limited insights into ant dietary specialization. Here we synthesize and analyze research on ant gustation to identify mechanisms, sociobiological correlates, and phylogenetic patterns. We discuss the current state of genomic analyses of taste and future research. We propose that strikingly polymorphic species of Pheidole , Cephalotes , Camponotus , and leafcutter ants ( Atta and Acromyrmex ) offer compelling social systems to explore adaptive variation in gustation because of their pronounced division of labor in which morphologically, behaviorally, and neurally differentiated workers vary in feeding behavior. Research on ant gustation within and among species will advance our understanding of sensory systems and provide insight into the impact of taste on the evolution of species diversity and how social organization influences gustation.
more »
« less
Topological constraints in early multicellularity favor reproductive division of labor
Reproductive division of labor (e.g. germ-soma specialization) is a hallmark of the evolution of multicellularity, signifying the emergence of a new type of individual and facilitating the evolution of increased organismal complexity. A large body of work from evolutionary biology, economics, and ecology has shown that specialization is beneficial when further division of labor produces an accelerating increase in absolute productivity (i.e. productivity is a convex function of specialization). Here we show that reproductive specialization is qualitatively different from classical models of resource sharing, and can evolve even when the benefits of specialization are saturating (i.e. productivity is a concave function of specialization). Through analytical theory and evolutionary individual-based simulations, we demonstrate that reproductive specialization is strongly favored in sparse networks of cellular interactions that reflect the morphology of early, simple multicellular organisms, highlighting the importance of restricted social interactions in the evolution of reproductive specialization.
more »
« less
- PAR ID:
- 10233727
- Date Published:
- Journal Name:
- eLife
- Volume:
- 9
- ISSN:
- 2050-084X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Eusociality represents an extreme form of social behavior characterized by a reproductive division of labor. Eusociality necessarily evolved through kin selection, which requires interactions among related individuals. However, many eusocial taxa also show cooperation between non-kin groups, challenging the idea that cooperative actions should only occur among relatives. This review explores the causes and consequences of non-kin cooperation in ants. Ants display a diversity of behaviors that lead to non-kin cooperation within and between species. These interactions occur among both reproductive and non-reproductive individuals. The proximate and ultimate mechanisms leading to non-kin cooperative interactions differ substantially depending on the biotic and abiotic environment. We end this review with directions for future research and suggest that the investigation of non-kin cooperative actions provides insight into processes leading to social evolution.more » « less
-
The emergence of new replicating entities from the union of simpler entities characterizes some of the most profound events in natural evolutionary history. Such transitions in individuality are essential to the evolution of the most complex forms of life. Thus, understanding these transitions is critical to building artificial systems capable of open-ended evolution. Alas, these transitions are challenging to induce or detect, even with computational organisms. Here, we introduce the DISHTINY (Distributed Hierarchical Transitions in Individuality) platform, which provides simple cell-like organisms with the ability and incentive to unite into new individuals in a manner that can continue to scale to subsequent transitions. The system is designed to encourage these transitions so that they can be studied: Organisms that coordinate spatiotemporally can maximize the rate of resource harvest, which is closely linked to their reproductive ability. We demonstrate the hierarchical emergence of multiple levels of individuality among simple cell-like organisms that evolve parameters for manually designed strategies. During evolution, we observe reproductive division of labor and close cooperation among cells, including resource-sharing, aggregation of resource endowments for propagules, and emergence of an apoptosis response to somatic mutation. Many replicate populations evolved to direct their resources toward low-level groups (behaving like multicellular individuals), and many others evolved to direct their resources toward high-level groups (acting as larger-scale multicellular individuals).more » « less
-
ABSTRACT Microbes face a trade-off between being metabolically independent and relying on neighboring organisms for the supply of some essential metabolites. This balance of conflicting strategies affects microbial community structure and dynamics, with important implications for microbiome research and synthetic ecology. A “gedanken” (thought) experiment to investigate this trade-off would involve monitoring the rise of mutual dependence as the number of metabolic reactions allowed in an organism is increasingly constrained. The expectation is that below a certain number of reactions, no individual organism would be able to grow in isolation and cross-feeding partnerships and division of labor would emerge. We implemented this idealized experiment using in silico genome-scale models. In particular, we used mixed-integer linear programming to identify trade-off solutions in communities of Escherichia coli strains. The strategies that we found revealed a large space of opportunities in nuanced and nonintuitive metabolic division of labor, including, for example, splitting the tricarboxylic acid (TCA) cycle into two separate halves. The systematic computation of possible solutions in division of labor for 1-, 2-, and 3-strain consortia resulted in a rich and complex landscape. This landscape displayed a nonlinear boundary, indicating that the loss of an intracellular reaction was not necessarily compensated for by a single imported metabolite. Different regions in this landscape were associated with specific solutions and patterns of exchanged metabolites. Our approach also predicts the existence of regions in this landscape where independent bacteria are viable but are outcompeted by cross-feeding pairs, providing a possible incentive for the rise of division of labor. IMPORTANCE Understanding how microbes assemble into communities is a fundamental open issue in biology, relevant to human health, metabolic engineering, and environmental sustainability. A possible mechanism for interactions of microbes is through cross-feeding, i.e., the exchange of small molecules. These metabolic exchanges may allow different microbes to specialize in distinct tasks and evolve division of labor. To systematically explore the space of possible strategies for division of labor, we applied advanced optimization algorithms to computational models of cellular metabolism. Specifically, we searched for communities able to survive under constraints (such as a limited number of reactions) that would not be sustainable by individual species. We found that predicted consortia partition metabolic pathways in ways that would be difficult to identify manually, possibly providing a competitive advantage over individual organisms. In addition to helping understand diversity in natural microbial communities, our approach could assist in the design of synthetic consortia.more » « less
-
Larracuente, Amanda (Ed.)Abstract The methyltransferase like (METTL) proteins constitute a family of seven-beta-strand methyltransferases with S-adenosyl methionine binding domains that modify DNA, RNA, and proteins. Methylation by METTL proteins contributes to the epigenetic, and in the case of RNA modifications, epitranscriptomic regulation of a variety of biological processes. Despite their functional importance, most investigations of the substrates and functions of METTLs within metazoans have been restricted to model vertebrate taxa. In the present work, we explore the evolutionary mechanisms driving the diversification and functional differentiation of 33 individual METTL proteins across Metazoa. Our results show that METTLs are nearly ubiquitous across the animal kingdom, with most having arisen early in metazoan evolution (i.e., occur in basal metazoan phyla). Individual METTL lineages each originated from single independent ancestors, constituting monophyletic clades, which suggests that each METTL was subject to strong selective constraints driving its structural and/or functional specialization. Interestingly, a similar process did not extend to the differentiation of nucleoside-modifying and protein-modifying METTLs (i.e., each METTL type did not form a unique monophyletic clade). The members of these two types of METTLs also exhibited differences in their rates of evolution. Overall, we provide evidence that the long-term evolution of METTL family members was driven by strong purifying selection, which in combination with adaptive selection episodes, led to the functional specialization of individual METTL lineages. This work contributes useful information regarding the evolution of a gene family that fulfills a variety of epigenetic functions, and can have profound influences on molecular processes and phenotypic traits.more » « less
An official website of the United States government

