bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434999; this version posted March 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Title: Understanding the Evolution of Nutritive Taste in Animals: Insights from Biological 2 Stoichiometry and Nutritional Geometry 3 Running title: Biological Stoichiometry, Nutrition and Taste 4 Authors: Lee M. Demi1*, Brad W. Taylor1, Benjamin J. Reading1, Michael G. Tordoff2, Robert 5 R. Dunn1,3 6 Affiliations: 7 1Department of Applied Ecology, North Carolina State University, Raleigh, NC 27695, USA 8 2 Monell Chemical Senses Center, Philadelphia, PA 19104, USA 9 3 Center for Evolutionary Hologenomics, University of Copenhagen, Copenhagen, DK 10 *Corresponding author: [email protected] 11 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434999; this version posted March 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 12 Abstract: 13 A major conceptual gap in taste biology is the lack of a general framework for understanding the 14 evolution of different taste modalities among animal species. We turn to two complementary 15 nutritional frameworks, biological stoichiometry theory and nutritional geometry, to develop 16 hypotheses for the evolution of different taste modalities in animals. We describe how the 17 attractive tastes of Na, Ca, P, N and C containing compounds are consistent with principles of 18 both frameworks based on their shared focus on nutritional imbalances and consumer 19 homeostasis. Specifically, we suggest that the evolution of multiple nutritive taste modalities can 20 be predicted by identifying individual elements that are typically more concentrated in the tissues 21 of animals than plants. Additionally, we discuss how consumer homeostasis can inform our 22 understanding of why some taste compounds (i.e., Na, Ca and P salts) can be either attractive or 23 aversive depending on concentration. We also discuss how these complementary frameworks can 24 help to explain the phylogenetic distribution of different taste modalities and improve our 25 understanding of the mechanisms that lead to loss of taste capabilities in some animal lineages. 26 The ideas presented here will stimulate research that bridges the fields of evolutionary biology, 27 sensory biology and ecology. 28 29 Keywords (5): gustation, nutritional ecology, chemoreception, homeostasis, optimal foraging 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434999; this version posted March 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 30 1. Introducing a general framework for consumptive taste evolution 31 All organisms are faced with the challenge of procuring the essential elements and biochemicals 32 of life for growth, maintenance and reproduction, often in proportions that deviate substantially 33 from their environmental availability. For animals, nutrients (i.e., elements and/or biochemicals) 34 are acquired through their diet by consuming foods that may vary considerably in their chemical 35 composition and that frequently provide an inadequate supply of one or more essential nutrient 36 (1). Thus, many animals suffer periodic nutritional imbalances whereby the nutrient content of 37 available foods does not match their nutritional requirements. Such imbalances (i.e., over- or 38 undersupply of essential nutrients) can affect consumer metabolism and performance, ultimately 39 resulting in reduced growth and fitness (2, 3). Because nutritional imbalances between 40 consumers and their foods are both pervasive and consequential animals have evolved a range of 41 adaptations, from behavioral to physiological and chemosensory, that allow them to modulate 42 nutrient intake, as well as post-ingestion nutrient processing (i.e., assimilation and allocation), to 43 minimize potential imbalances (3). 44 Selective foraging is a key behavioral adaptation that allows animals to regulate nutrient 45 intake in order to achieve balanced nutrient supply (3). Choosing exactly which foods to eat, 46 however, requires that animals differentiate among potential food sources of differing chemical 47 composition to select those that are most nutritionally advantageous. One of the primary 48 mechanisms that animals use to assess the nutritional quality of foods is gustation, or taste, 49 which provides animals the ability to evaluate the chemical composition of potential foods prior 50 to ingestion via complex chemosensory systems (4, 5, 6). Indeed, there is broad recognition that 51 gustatory systems function primarily as a screening mechanism that drives consumption of 52 nutrient- and energy-dense foods, as well as the rejection of potentially harmful ones based upon 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434999; this version posted March 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 53 the presence, and concentrations, of a variety of different chemicals. These various chemical 54 stimuli interact with specialized receptor cells to produce signals that are transduced and 55 interpreted as unique taste modalities, including the salty, sweet, bitter, sour and umami tastes 56 familiar to humans (4, 6). 57 The variety of different taste modalities provide organisms with a way to evaluate the 58 quality of food based on multiple aspects of its chemical composition and can be broadly 59 grouped by whether they taste “good”, and therefore promote consumption, or “bad”, thus 60 producing an aversive response. Consumptive responses, such as those elicited by sweet and 61 umami tastes, promote the ingestion of foods that supply compounds essential for growth and 62 metabolism. Conversely, aversive responses, such as those typically generated by bitter and sour 63 tastes, encourage animals to reject, rather than consume specific foods. Aversive tastes are 64 generally thought to inform consumers that food may contain toxic or harmful chemicals, such as 65 allelochemicals, though not all chemicals that produce innate aversive responses are necessarily 66 harmful (5, 6). Additionally, some elements, such as Na, Ca and P which are essential but can be 67 toxic when oversupplied, may elicit either consumptive or aversive responses depending on 68 concentration, thereby allowing consumers to regulate intake within a relatively narrow window. 69 All animals possess gustatory sensing capabilities (3, 7), reinforcing the notion that 70 regulation of nutrient intake is highly consequential for consumer fitness. Interestingly, gustatory 71 sensing appears to have evolved largely independently among prominent animal lineages (i.e., 72 mammals and insects) (5), yet exhibits remarkable convergence around taste capabilities for a 73 small suite of compounds (e.g., amino acids, carbohydrates, Na salts). This suggests that animals 74 have faced similar nutritional constraints throughout their evolutionary history and indicates 75 potential for developing a nutritional framework for understanding the evolution of taste that has 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.03.11.434999; this version posted March 12, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 76 broad applicability. Nevertheless, we currently lack a predictive understanding of when and why 77 particular taste modalities might be evolutionarily favored (3), thereby leading to differences in 78 the breadth of gustatory capabilities among species. 79 In this paper, we turn to two complementary frameworks, biological stoichiometry theory 80 (2, 8, 9) and nutritional geometry (1, 3, 10), that have been developed by ecologists to 81 characterize nutritional imbalances (and their consequences) in trophic interactions to draw 82 insights into the evolutionary contexts under which different taste modalities have evolved in 83 animals. In the following sections, we summarize the basic tenets of biological stoichiometry 84 theory and nutritional geometry, including the unifying concept of consumer homeostasis, and 85 draw upon a review of the taste biology literature to show how these complementary frameworks 86 advance our understanding of the evolution of multiple taste modalities in animals. We use the 87 principles of biological stoichiometry to demonstrate that the evolution of multiple nutritive taste 88 modalities can be predicted by identifying individual elements that are typically more 89 concentrated in the tissues of animals than plants. Moreover, we describe how consumer 90 homeostasis can inform our understanding of why some taste compounds (i.e., Na, Ca and P 91 salts) can be either attractive or aversive depending on concentration. Additionally, we 92 demonstrate how these complementary frameworks can help to explain the phylogenetic 93 distribution of different taste modalities, including why the taste of Ca (at least at some 94 concentrations) is attractive to some vertebrate species but appears to be strictly aversive to 95 insects. We also discuss how biological stoichiometry and nutritional geometry can improve