Abstract
High mating success in animals is often dependent on males signalling attractively with high effort. Since males should be selected to maximize their reproductive success, female preferences for these traits should result in minimal signal variation persisting in the population. However, extensive signal variation persists. The genic capture hypothesis proposes genetic variation persists because fitness-conferring traits depend on an individual's basic processes, including underlying physiological, morphological, and biochemical traits, which are themselves genetically variable. To explore the traits underlying signal variation, we quantified among-male differences in signalling, morphology, energy stores, and the activities of key enzymes associated with signalling muscle metabolism in two species of crickets, Gryllus assimilis (chirper: <20 pulses/chirp) and G. texensis (triller: >20 pulses/chirp). Chirping G. assimilis primarily fuelled signalling with carbohydrate metabolism: smaller individuals and individuals with increased thoracic glycogen stores signalled for mates with greater effort; individuals with greater glycogen phosphorylase activity produced more attractive mating signals. Conversely, the more energetic trilling G. texensis fuelled signalling with both lipid and carbohydrate metabolism: individuals with increased β-hydroxyacyl-CoA dehydrogenase activity and increased thoracic free carbohydrate content signalled for mates with greater effort; individuals with higher thoracic and abdominal carbohydrate content and higher abdominal lipid stores produced more attractive signals. Our findings suggest variation in male reproductive success may be driven by hidden physiological trade-offs that affect the ability to uptake, retain, and use essential nutrients, although the results remain correlational in nature. Our findings indicate that a physiological perspective may help us to understand some of the causes of variation in behaviour.
Highlights
The lek paradox refers to the puzzle of how male sexual traits continually exhibit extensive genetic variation even though female preferences should cause its rapid decline [1,2,3,4]
The most notable differences in enzyme activity were for GP and hydroxyacyl-CoA dehydrogenase (HOAD), with males displaying 22- and 16-fold differences, respectively
Our findings suggest that the ability to mobilize and/or metabolize glycogen in G. assimilis and free carbohydrates and lipids in G. texensis may underlie some of the intraspecific signalling variation observed in nature
Summary
The lek paradox refers to the puzzle of how male sexual traits continually exhibit extensive genetic variation even though female preferences should cause its rapid decline [1,2,3,4]. Genic capture posits that preferred traits are highly genetically variable because they depend on many underlying physiological, morphological, and biochemical traits that affect condition [3]. Genic capture rests on the assumption that genetic variation in condition drives variation in preferred traits. In a recent perspective article, Hill [9] defined condition as ‘‘the relative capacity to maintain optimal functionality of essential cellular processes’’. He argued that condition is influenced by genotype, epigenetic state, and somatic state. Hill [9] called upon behavioural ecologists to ascertain whether expression of preferred traits reflects a capacity to remain near an optimal state. We explore the cellular processes linked to preferred trait production using field crickets (Orthoptera: Gryllidae) as model organisms
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