An official website of the United States government
Abstract Concerted developmental programming may constrain changes in component structures of the brain, thus limiting the ability of selection to form an adaptive mosaic of size‐variable brain compartments independent of total brain size or body size. Measuring patterns of gene expression underpinning brain scaling in conjunction with anatomical brain atlases can aid in identifying influences of concerted and/or mosaic evolution. Species exhibiting exceptional size and behavioral polyphenisms provide excellent systems to test predictions of brain evolution models by quantifying brain gene expression. We examined patterns of brain gene expression in a remarkably polymorphic and behaviorally complex social insect, the leafcutter antAtta cephalotes. The majority of significant differential gene expression observed among three morphologically, behaviorally, and neuroanatomically differentiated worker size groups was attributable to body size. However, we also found evidence of differential brain gene expression unexplained by worker morphological variation and transcriptomic analysis identified patterns not linearly correlated with worker size but sometimes mirroring neuropil scaling. Additionally, we identified enriched gene ontology terms associated with nucleic acid regulation, metabolism, neurotransmission, and sensory perception, further supporting a relationship between brain gene expression, brain mosaicism, and worker labor role. These findings demonstrate that differential brain gene expression among polymorphic workers underpins behavioral and neuroanatomical differentiation associated with complex agrarian division of labor inA. cephalotes.
more »
« less
Social Brain Energetics: Ergonomic Efficiency, Neurometabolic Scaling, and Metabolic Polyphenism in Ants
Abstract Metabolism, a metric of the energy cost of behavior, plays a significant role in social evolution. Body size and metabolic scaling are coupled, and a socioecological pattern of increased body size is associated with dietary change and the formation of larger and more complex groups. These consequences of the adaptive radiation of animal societies beg questions concerning energy expenses, a substantial portion of which may involve the metabolic rates of brains that process social information. Brain size scales with body size, but little is understood about brain metabolic scaling. Social insects such as ants show wide variation in worker body size and morphology that correlates with brain size, structure, and worker task performance, which is dependent on sensory inputs and information-processing ability to generate behavior. Elevated production and maintenance costs in workers may impose energetic constraints on body size and brain size that are reflected in patterns of metabolic scaling. Models of brain evolution do not clearly predict patterns of brain metabolic scaling, nor do they specify its relationship to task performance and worker ergonomic efficiency, two key elements of social evolution in ants. Brain metabolic rate is rarely recorded and, therefore, the conditions under which brain metabolism influences the evolution of brain size are unclear. We propose that studies of morphological evolution, colony social organization, and worker ergonomic efficiency should be integrated with analyses of species-specific patterns of brain metabolic scaling to advance our understanding of brain evolution in ants.
more »
« less
- Award ID(s):
- 2141592
- PAR ID:
- 10368214
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- ISSN:
- 1540-7063
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Human brain size nearly quadrupled in the six million years since Homo last shared a common ancestor with chimpanzees, but human brains are thought to have decreased in volume since the end of the last Ice Age. The timing and reason for this decrease is enigmatic. Here we use change-point analysis to estimate the timing of changes in the rate of hominin brain evolution. We find that hominin brains experienced positive rate changes at 2.1 and 1.5 million years ago, coincident with the early evolution of Homo and technological innovations evident in the archeological record. But we also find that human brain size reduction was surprisingly recent, occurring in the last 3,000 years. Our dating does not support hypotheses concerning brain size reduction as a by-product of body size reduction, a result of a shift to an agricultural diet, or a consequence of self-domestication. We suggest our analysis supports the hypothesis that the recent decrease in brain size may instead result from the externalization of knowledge and advantages of group-level decision-making due in part to the advent of social systems of distributed cognition and the storage and sharing of information. Humans live in social groups in which multiple brains contribute to the emergence of collective intelligence. Although difficult to study in the deep history of Homo , the impacts of group size, social organization, collective intelligence and other potential selective forces on brain evolution can be elucidated using ants as models. The remarkable ecological diversity of ants and their species richness encompasses forms convergent in aspects of human sociality, including large group size, agrarian life histories, division of labor, and collective cognition. Ants provide a wide range of social systems to generate and test hypotheses concerning brain size enlargement or reduction and aid in interpreting patterns of brain evolution identified in humans. Although humans and ants represent very different routes in social and cognitive evolution, the insights ants offer can broadly inform us of the selective forces that influence brain size.more » « less
-
Abstract Females and males can exhibit striking differences in body size, relative trait size, physiology, and behavior. As a consequence, the sexes can have very different rates of whole-body energy use, or converge on similar rates through different physiological mechanisms. Yet many studies that measure the relationship between metabolic rate and body size only pay attention to a single sex (more often males), or do not distinguish between sexes. We present four reasons why explicit attention to energy-use between the sexes can yield insight into the physiological mechanisms that shape broader patterns of metabolic scaling in nature. First, the sexes often differ considerably in their relative investment in reproduction, which shapes much of life-history and rates of energy use. Second, males and females share a majority of their genome but may experience different selective pressures. Sex-specific energy profiles can reveal how the energetic needs of individuals are met despite the challenge of within-species genetic constraints. Third, sexual selection often pushes growth and behavior to physiological extremes. Exaggerated sexually selected traits are often most prominent in one sex, can comprise up to 50% of body mass, and thus provide opportunities to uncover energetic constraints of trait growth and maintenance. Finally, sex-differences in behavior such as mating-displays, long-distance dispersal, and courtship can lead to drastically different energy allocation among the sexes; the physiology to support this behavior can shape patterns of metabolic scaling. The mechanisms underlying metabolic scaling in females, males, and hermaphroditic animals can provide opportunities to develop testable predictions that enhance our understanding of energetic scaling patterns in nature.more » « less
-
null (Ed.)Social insects exhibit highly variable body plans at multiple scales: within colonies, between conspecific colonies, and across different species. The interspecific variation in the existence and prevalence of morphologically discrete worker subcastes in social insects raises questions about the ontogeny and functional importance of alternative worker body plans. Here, we examine the allometry of four Formica species. Formica are among the most common ants in the northern hemisphere temperate zone, and species vary greatly in the degree of worker size variation. However, no Formica species exhibit obvious worker subcastes. By carefully measuring head width, head height, scape length, thorax length, hind femur length, and hind tibia length in 180 individuals, we confirm that Formica workers exhibit continuous linear scaling, meaning that they lack discrete morphological subcastes. Most measurements scale allometrically. Different colonies of the same species are generally consistent in the slope of these relationships, and we detect unexpected similarities in scaling relationships among the four Formica species as well. Some scaling relationships, including a proportionally shorter scape and larger head in large-bodied workers, were also previously found in fire ants. Identifying worker size and shape distributions among different species is a vital step in understanding the selection pressures shaping division of labor in insect societies.more » « less
-
Body size covaries with population dynamics across life’s domains. Metabolism may impose fundamental constraints on the coevolution of size and demography, but experimental tests of the causal links remain elusive. We leverage a 60,000-generation experiment in which Escherichia coli populations evolved larger cells to examine intraspecific metabolic scaling and correlations with demographic parameters. Over the course of their evolution, the cells have roughly doubled in size relative to their ancestors. These larger cells have metabolic rates that are absolutely higher, but relative to their size, they are lower. Metabolic theory successfully predicted the relations between size, metabolism, and maximum population density, including support for Damuth’s law of energy equivalence, such that populations of larger cells achieved lower maximum densities but higher maximum biomasses than populations of smaller cells. The scaling of metabolism with cell size thus predicted the scaling of size with maximum population density. In stark contrast to standard theory, however, populations of larger cells grew faster than those of smaller cells, contradicting the fundamental and intuitive assumption that the costs of building new individuals should scale directly with their size. The finding that the costs of production can be decoupled from size necessitates a reevaluation of the evolutionary drivers and ecological consequences of biological size more generally.more » « less
