Mitochondrial function, ornamentation, and immunocompetence

Abstract

Understanding the mechanisms that link ornamental displays and individual condition is key to understanding the evolution and function of ornaments. Immune function is an aspect of individual quality that is often associated with the expression of ornamentation, but a general explanation for why the expression of some ornaments seems to be consistently linked to immunocompetence remains elusive. We propose that condition-dependent ornaments may be linked to key aspects of immunocompetence through co-dependence on mitochondrial function. Mitochondrial involvement in immune function is rarely considered outside of the biomedical literature, but the role of mitochondria as the primary energy producers of the cell and the centres of biosynthesis, the oxidative stress response, and cellular signalling place them at the hub of a variety of immune pathways. A promising new mechanistic explanation for correlations between a wide range of ornamental traits and the properties of individual quality is that mitochondrial function may be the 'shared pathway' responsible for links between ornament production and individual condition. Herein, we first review the role of mitochondria as both signal transducers and metabolic regulators of immune function. We then describe connections between hormonal pathways and mitochondria, with implications for both immune function and the expression of ornamentation. Finally, we explore the possibility that ornament expression may link directly to mitochondrial function. Considering condition-dependent traits within the framework of mitochondrial function has the potential to unify central tenets within the study of sexual selection, eco-immunology, oxidative stress ecology, stress and reproductive hormone biology, and animal physiology.

Do carotenoid‐based ornaments entail resource trade‐offs? An evaluation of theory and data

“…Briefly, carotenoids have been implicated in lymphocyte proliferation and activity, though their biochemical participation in such processes remains uncertain (Chew & Park, ). It is possible that carotenoids may be localized to specific organelles, such as the mitochondria, where they may prevent oxidative damage and therefore facilitate proper cellular function in immune cells (Chew & Park, ; Hill, ; Koch, Josefson, & Hill, )—but this hypothesis remains to be tested. Carotenoids have also been cited as important to preventing damage to self during the innate immune process of oxidative burst in which immune cells target pathogens for oxidative damage by rapidly releasing pro‐oxidants (Chew & Park, ), though the process functions differently in mammalian vs. avian cells (Harmon, ), and thus far there is little evidence to suggest a role of carotenoids in oxidative burst in birds (Koch et al., ; Sild, Sepp, Manniste, & Horak, ).…”

How to measure mitochondrial function in birds using red blood cells: a case study in the king penguin and perspectives in ecology and evolution

“…; Schwartz, Arendsee & Bronikowski ; Bar‐Yaacov et al . ; Koch, Josefson & Hill ; Delhaye et al . ).…”

Mitonuclear Mate Choice: A Missing Component of Sexual Selection Theory?

“…Poor function of cellular respiratory systems can be a product of genotype (including mt or N genes), environment, or the interaction of genotype and environment . A variety of environmental perturbations is known to disrupt mitochondrial function, particularly in humans but also for a range of eukaryotes . In addition, a large number of named inherited diseases involve either mt or N‐mt genes and affect mitochondrial function .…”

“…A range of traits such as patches of color, rates of songs, amplitude of calls, flight displays, pheromone quantity, and cognitive ability have been documented to be honest signals of individual condition . The origins of condition dependency in ornamental traits has been the subject of speculation and debate for decades, but a new hypothesis proposes that production of condition‐dependent traits is directly linked to energy production and oxidative state and hence to mitochondrial function . Through such mate choice for condition‐dependent ornaments, choosing individuals would not only avoid poorly functioning combinations of N‐mt and mt genes, but they would also avoid mates that have functional OXPHOS gene combinations but that have been compromised by poor diet, parasites, and other environmental challenges .…”

“…[73,74] A variety of environmental perturbations is known to disrupt mitochondrial function, particularly in humans but also for a range of eukaryotes. [75,76] In addition, a large number of named inherited diseases involve either mt or N-mt genes and affect mitochondrial function. [77,78] It is estimated that one in 400 people carries pathogenic (mtDNA) mutations.…”