Evolutionary physiology at 30+: Has the promise been fulfilled?

The evolution of honest signals has a physiological basis

Biological communication is mainly driven by signals, traits that evolve because of the benefits obtained by their recipients.[81] When signals can allow the Darwinian fitness (reproductive success) of their recipients to improve, they are considered “honest.” This appears to be the case for most biological traits that fulfill a signaling role.[82] Signal honesty is closely related to the concept of individual quality. As stated in the handicap principle, a cornerstone of behavioral ecology, the production of large (expensive) signals is limited to high-quality signalers because low-quality ones cannot afford the costs derived from signal production.[83] However, this explanation has been challenged in recent years because costs for low-quality individuals are frequently not found in empirical studies, and, indeed, natural selection is not expected to favor the evolution of signals when it implies incurring substantive costs.[84] As a consequence, the existence of costs predicted by the handicap principle is not fully accepted by evolutionary biology, which currently lacks an integrated approach to explain the concept of individual quality and the evolution of honesty.

Recent physiological experiments on the classical honest signaling system of the black bib of male house sparrows (Passer domesticus) illustrate the possibility that costs are not necessary to explain why low-quality individuals do not develop high-quality signals (i.e., large bibs). Large bibs are associated with low amounts of the pigment pheomelanin in their constitutive feathers, which allows researchers to experimentally create physiological conditions that favor the production of small or large bibs by exposing birds to substances that act as inhibitors or enhancers of pheomelanin synthesis.[85] Despite these induced physiological conditions, the resulting phenotype could be manipulated in high-quality birds (i.e., those with largest bibs initially) only. A physiological mechanism may therefore exist in low-quality individuals that make them less sensitive to environmental factors than high-quality individuals, which prevents low-quality individuals from producing high-quality signals even if they took the “decision” to do so or if environmental conditions favored the production of large signals.[85]

The experiments on the signaling system of male house sparrows exemplify how the details of the machinery controlling the expression of signals can explain their honesty without the costs predicted by the handicap principle. Although specific to visual traits whose production is mediated by the synthesis of melanin pigments, these experiments show that the evolution of honesty can have a physiological basis. Similar studies on the physiological basis of trait production in other honest signaling systems, including those in humans,[86] may provide a more general concept of individual quality and consequently represent a new understanding of this aspect of biological communication.

Elucidating the physiological underpinnings of evolutionary adaptations

As evolutionary adaptations directly depend on functional aspects of organisms, physiology, and related fields have the potential to provide a conjectural background to understand them (e.g., see [87]). A diversity of approaches in evolutionary physiology can be used to identify the mechanisms by which adaptations arise (e.g., see [6, 12, 13, 18, 35, 37, 65, 68]). These approaches include direct gene editing of genes underlying adaptations, genomic analyses of phenotypes resulting from selection (natural, artificial, or experimental), contrasting repeated evolutionary events of physiological phenotypes using physiological experiments, and the application of physiological knowledge to evolutionary adaptations. We provide examples for these below and in Box 1, including simple economical ideas that have been used to understand the evolution of pigmentation phenotypes[88] and theories of sensory cue integration to understand the evolution of perception capacity.[89]

Box 1. The use of cross-organism integration to understand physiological evolution

The use of wild species and the integration of findings across organisms is a powerful but underutilized approach to understanding physiological evolution. Here we provide two examples of how we think this has been done well and can provide road maps for others to utilize this approach.

Example 1: Tracking metabolic pathways in different organisms, for example, provides insight into the adaptive value of metabolic products. This is the case of biological pigments, whose whole chemical diversity can be categorized into three common synthesis routes after tracking them across all organisms, suggesting common functional roles.[131] Melanins, pigments that are the result of one of these routes, are probably synthesized by all organisms. From bacteria to humans, broad optical absorption properties make melanins exert a universal protecting role against cellular damage caused by solar UV radiation.[132] Carotenoid pigments resulting from another synthesis route, are synthesized by photosynthetic organisms that benefit from the charge transfer properties of these pigments, which facilitate photosynthesis under exposure to sunlight. Animals that take carotenoids with food, such as insects,[133] benefit from the same properties to quench free radicals and possibly from enhancing properties of the mitochondrial function and thus protect cells from oxidative stress[134] as do birds and other organisms as the cartenoids pass up the food chain.[135] Lastly, porphyrins, pigments corresponding to the third route, fulfill a key role in all vertebrates by acting as intermediates in the synthesis of heme.[130] Marine invertebrates also synthesize porphyrins, and although their physiological role in these groups is unknown, it is likely to be related to the essential role exerted in vertebrates.[136]

Example 2. The mechanistic basis of evolutionary adaptations to high altitude and hypoxia resistance has been informed by genomics studies across species, from mammals and birds to insects.[137-139] The integrated knowledge across these studies reveals the commonalities of approaches that evolution has taken and thereby revealing the higher-order constraints in the physiological system. Compiled across species, the genes underlying the physiological processes of oxygen transport, metabolic processes, and the hypoxia-inducible factor pathway are some of the most prominent targets of selection for living in high altitude environments. In some cases, the same genes are being targeted across species, in other cases different genes in the same process are targets. Genetic variants in and around these genes have been found to be segregating across high and low-altitude populations, and functional studies have demonstrated their importance. Contrasting across these studies reveal the diversity of mechanisms that has been used by evolution to manipulate hypoxia tolerance at many biological levels to achieve similar adaptive benefits to living at high altitude conditions. In some species and populations, the genetic variants differentially regulate transcription of the genes in response to the high-altitude, and thereby altering the amount of the protein product produced in those conditions relative to low-altitude species; in other cases, they alter the amino acid sequence to affect the function of the protein. To illustrate these points, in the figure below we highlight a small subset of the genetic variants that have been identified across different species involved in the evolutionary adaptation to living in high altitude environments (see more extensive reviews[137-139]).

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Research methods in physiology have always strongly relied on experimental manipulations of biological processes[90] and the advent of molecular tools, such as CRISPR, allow manipulations at the level of the genome to prove physiological mechanisms. Although evolutionary adaptations have been linked to specific genes in a growing number of cases (e.g., [7, 91-93]), typically these genes fit in to molecular networks — interactions among genes, proteins, and RNAs that are coordinated within the cell — to regulate physiological outcomes. Selection acting on a larger network makes it much harder to detect effects on particular loci because the impact can be shared across loci with relatively small effect, and the probability of pleiotropic effects is high in a network. Moreover, the experimental manipulation of multiple genes concurrently to understand their physiological effects is much more difficult than changing single genes.

Rather than attempting to manipulate genes directly, selection experiments focused at behavioral or other whole-organism levels can be used to understand how evolution can bring about adaptations through shaping of a molecular network. Dogs are a great example, having been under artificial selection for thousands of years, resulting in breeds defined by form, function, and behavior.[94] The evolutionary response to selection that targeted growth, strength, and body size has involved the insulin and insulin-like signaling (IIS) network.[95] This molecular network integrates over 100 genes, and this network has been studied extensively for its pleiotropic effects on both early (growth and reproduction) and late life (rate of aging) traits in various model organisms.[96] Selection has sorted alleles by dog breed for at least seven loci, and most of these genes are in or related to the IIS network.[95] The allelic variation at these seven loci explains over 50% of the variation in body size among breeds. Together, in the context of the function of the IIS network on the cellular and organismal physiology, the alleles in the small-bodied breeds (e.g., Chihuahua) reduce the cellular signaling through IIS network resulting in the correlated phenotypes of small body, small litters, and longer lifespans relative to the larger breeds (e.g., Mastiff).[95, 97]

Sensory systems also provide clear illustrations of how physiological knowledge helps us to understand evolutionary adaptations (see also examples in [6]). In the most general sense, the sensory perception of organisms depends on their physiological allocation to the systems involved. This physiological allocation differs among species and even individuals, but this does not mean that perceived objects are only the product of neuronal activity or that the brain produces realistic models without capturing reality itself. The chromatic experience of animals, for example, is not only a type of neural state or process, but also reflects to a large degree the color of the objects being perceived as a physical attribute of these objects. Color perception is thus the combination of an objective and a subjective experience, the latter greatly influencing the ecological/evolutionary implications of perceiving the color of given objects.[98] Color interpretation in some evolutionary studies has been made in a way that gives much weight to the subjective component of color perception (e.g., “Color is not an inherent property of the object; it is a product of the brain of the animal perceiving the object,”[99]), but it must be remembered that color is also a physical attribute of the objects. Considering the objective component of color perception may be useful in interspecific comparisons of animal coloration, and thus provide clues into the adaptiveness of color traits. Indeed, human vision can detect much of the variation in bird coloration in the visible range and also provide a valid proxy for avian perception of such color traits as sexual dichromatism,[100, 101] suggesting that considering color exclusively as a neural state may be an incomplete view. That color resides in both the objects being perceived and in the brain of the perceiving animals is known in neuroscience since the 1990s, notably through the work of Francisco J. Varela and others.[98, 102] Considering this theoretical background of sensory physiology may therefore help in gaining a deeper insight into the adaptive value of color phenotypes.

In addition statistical analyses are essential to detect patterns in physiological data.[90] It is important, however, that evolutionary inferences from physiological data are not exclusively dependent on statistics, in the sense of using only data that are devoid of clear functional, physiological meaning. Evolutionary biologists should take advantage of research approaches in physiology and related functional fields that allow less dependence on statistics. For example, several studies have reconstructed ancestral proteins and measured or inferred their functional characteristics to gain insight regarding physiological adaptation (e.g., [103, 104]).

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