Understanding the evolution of nutritive taste in animals: Insights from biological stoichiometry and nutritional geometry

Abstract

A major conceptual gap in taste biology is the lack of a general framework for understanding the evolution of different taste modalities among animal species. We turn to two complementary nutritional frameworks, biological stoichiometry theory and nutritional geometry, to develop hypotheses for the evolution of different taste modalities in animals. We describe how the attractive tastes of Na-, Ca-, P-, N-, and C-containing compounds are consistent with principles of both frameworks based on their shared focus on nutritional imbalances and consumer homeostasis. Specifically, we suggest that the evolution of multiple nutritive taste modalities can be predicted by identifying individual elements that are typically more concentrated in the tissues of animals than plants. Additionally, we discuss how consumer homeostasis can inform our understanding of why some taste compounds (i.e., Na, Ca, and P salts) can be either attractive or aversive depending on concentration. We also discuss how these complementary frameworks can help to explain the evolutionary history of different taste modalities and improve our understanding of the mechanisms that lead to loss of taste capabilities in some animal lineages. The ideas presented here will stimulate research that bridges the fields of evolutionary biology, sensory biology, and ecology.

Keywords: chemoreception; gustation; homeostasis; nutritional ecology; optimal foraging.

FIGURE 1

Carbon:nitrogen and carbon:phosphorus ratios of biomass across multiple trophic levels. Circles represent median values, and error bars indicate ranges of C:N and C:P observed for organisms within each trophic level. Autotroph data are from Elser et al. (9), where Autotroph (Plants) includes measurements of foliar chemistry of terrestrial autotrophs (for C:N, n = 406; for C:P, n = 413) and Autotroph (Plankton*) represents nutrient chemistry of seston from freshwater lakes (for C:N, n = 267; for C:P, n = 273). Seston contains some detritus and heterotrophic biomass (i.e., bacteria, protozoa) but is typically dominated by phytoplankton (9). Consumer stoichiometry data are from Vanni et al. (2017) and represent primarily aquatic animals. Data include 190 families from 9 animal phyla (herbivore and detritivore, n = 168; omnivore, n = 77; predator, n = 163)

FIGURE 2

The ratio of biomass concentrations of biologically “essential” elements in animals and plants for all elements which are at least 0.1% of dry mass in animals. Mass ratio is calculated as X _A/X _P, where X _A and X _P represent the % of dry mass for element X in animals and plants, respectively. Thus, values >1 indicate elements that are more concentrated in animal than plant tissues, 1 indicates equal concentrations, and values <1 indicate greater concentrations in plant tissue. Circles containing elemental symbols represent the average of data from mammals (orange), insects (black), and fish (blue) compiled by Bowen (Bowen, 1966 and 1979). Data for plants are from Markert (1992) and represent the elemental composition of foliar material