Behavioural mating displays depend on mitochondrial function: a potential mechanism for linking behaviour to individual condition

Abstract

Males of many animal species court females using complex behavioural displays that are challenging to produce, and some of these displays have been shown to be associated with aspects of male quality. However, the mechanisms by which behavioural displays are linked to individual condition remain uncertain. Herein, we illustrate fundamental mechanistic connections between mitochondrial function and neurogenesis, energy production, and a variety of pathways that underlie the ability of an individual to perform complex behaviours. We consider the biomedical evidence for how mitochondrial activity shapes neurogenesis during development and neural function in adulthood, and how both genetics and environmental conditions can cause variation in mitochondrial function in wild animals. An individual's mitochondrial phenotype determines not just metabolism and available energy, but also appears to serve as an important driver of capacity to perform cognitively complex and other challenging display behaviours. We apply this concept to the example of birdsong, a well-studied display behaviour with known links to neural pathways, and we describe how mitochondrial involvement in a variety of important internal processes creates links between display quality and key traits like immunocompetence. By synthesizing the intimate involvement of mitochondria in neural processes with the physiological bases of display behaviour, we aim to provide new mechanistic explanations for information that females may gain by assessing complex male displays.

Overexpression of an antioxidant enzyme improves male mating performance after stress in a lek-mating fruit fly

“…A recent synthesis of the biomedical literature by Koch & Hill [9] proposes that sexually selected behavioural displays are dependent on mitochondrial function, and our experiments provide experimental evidence in support of this hypothesis. Our results are consistent with previous work that oxidative stress and condition-dependent sexual traits are tightly linked [5][6][7].…”

Mother’s curse and indirect genetic effects: Do males matter to mitochondrial genome evolution?

“…Nuclear genetic variance in male‐induced harm has been demonstrated for D. melanogaster, and this nuclear indirect genetic effect explains a significant proportion of the variance in female egg production (Filice & Long, ). Similar variance stemming from the mitochondrial genome is plausible given the energetically demanding courtship behaviour of D. melanogaster males, and the close association between mtDNA and respiration (Dowling & Adrian, ; Koch & Hill, ; Liu, Fiskum, & Schubert, ).…”

Positive allometry of sexually selected traits: Do metabolic maintenance costs play an important role?

“…[124] Promising recent perspectives posit that mitochondrial function affects neurogenesis, energy production and the ability to perform complex displays suggesting a mechanistic link between behavior and metrics of condition. [55] To more fully integrate the study of exaggerated sexually selected traits and displays, it is critical to understand how energetic costs scale with body size. For example, large male wolf spiders pay about the twice the metabolic cost per-gram compared to small males during metabolically expensive drumming displays, yet these large males are able to sustain these disproportionately increased costs for short periods.…”

“…[ 30 ] Yet, sexually selected traits that do incur maintenance costs provide an avenue for these traits to be causally linked to an index of individual quality, [ 11 ] and these costs may serve as an honest indicator of competitive ability or a signal of quality. [ 55,56 ] However, because these maintenance costs are often relatively cheaper for larger individuals, this provides a mechanism for large individuals to invest in larger sexually selected traits because they pay relatively lower maintenance costs. To more fully understand the ways in which energetic demands of sexually selected traits may impose fitness costs, it is important to consider the demands of these tissues in the context of whole‐body energy budgets.…”

“…[ 124 ] Promising recent perspectives posit that mitochondrial function affects neurogenesis, energy production and the ability to perform complex displays suggesting a mechanistic link between behavior and metrics of condition. [ 55 ]…”