Income and capital breeding in males: energetic and physiological limitations on male mating strategies

Abstract

Income and capital breeding describe two dichotomous breeding strategies that characterise the allocation of resources to reproduction. Capital breeders utilise stored endogenous resources (typically lipids) to finance reproduction, whereas income breeders use exogenous resources (typically carbohydrates). The basis for such characterisation has mainly come from studying females, yet for many species, male and female reproductive success may be determined by substantially different factors. Females allocate resources to offspring production, whereas males typically allocate resources to accessing mating opportunities, e.g. from contests or displays. The primary metabolic fuel (lipids or carbohydrates) in males appears to be dependent on the type of activity being performed (i.e. high versus low intensity or long versus short duration), rather than capital or income breeding strategy per se. Males performing sustained, long-duration effort typically utilise lipids, whereas those undergoing intense activity more often utilise carbohydrates. As a result, either fuel type can be used in either strategy. Breeding season duration can constrain strategy choice; lipids and carbohydrates can be used in short breeding season species, but only lipids provide a viable fuel source for long breeding season capital breeders. Both capital-and income-breeding males must manage their resource use during the breeding season, but capital breeders must also cope with physiological stressors associated with extended fasting. Overall, the capital-income breeding concept applies equally to male reproduction, but compared with females, there are different physical and physiological constraints that shape choice of strategy. This Commentary also highlights some key future areas that need to be investigated to further understand how capital-income breeding strategies shape male mating strategies.

Does Physical Activity Age Wild Animals?

“…Barnacle geese Branta leucopsis make migratory flights lasting around 60 h in total during which their heart rates are ∼60% maximum (Butler et al, 1998), representing moderate exercise of long duration. In contrast, activities such as flight takeoff, predator avoidance, mating displays and active predation typically involve rates of energy expenditure at least several-fold that at rest (Vehrencamp et al, 1989;Green et al, 2009;Lane et al, 2010;Soulsbury, 2019), and can only be performed for short periods (Piersma, 2010). Exercise can be broadly characterized by three interacting components: (1) Intensity characterizes the percentage of oxygen consumption rate (VO 2 ) or heart rate relative to that at peak power output.…”

Protein Stores Regulate When Reproductive Displays Begin in the Male Caribbean Fruit Fly

“…Many animals rely on some combination of nutrient capital and income, and can regulate their behavior based on whether they have adequate nutrient stores to support reproduction (Frisch, 1985;Yin et al, 1999;Teal et al, 2013;Lebreton et al, 2017). The connection between fat storage and female fertility is well known, but our understanding of the relationships between male reproductive behavior and stored nutrition is incomplete (Mirth and Piper, 2017;Soulsbury, 2019). Although fat stores and leptin are reported to promote puberty in vertebrate males, the evidence from humans and rodents is still mixed and excessive fat stores may even inhibit reproduction (Zhang and Gong, 2018).…”

“…Many male reproductive displays require expensive signals (Soulsbury, 2019). Expensive signals can range from development of pre-breeding ornaments to pheromone-producing machinery to energetic fuel for behavioral displays.…”

“…Animals require nutrients for expensive life history transitions, especially reproductive maturation and engaging in nutrient-intensive reproductive behaviors ( Houston et al, 2006 ; Harshman and Zera, 2007 ; Soulsbury, 2019 ). However, many animals live in nutrient-limited environments, and the availability of abundant nutrient sources may not match a time and place well-suited for reproductive behavior (e.g., Ubukata, 1984 ; Warner, 1987 ; Yuval and Bouskila, 1993 ; Soulsbury, 2019 ). Accordingly, animals have evolved strategies to mitigate this problem.…”

Capital-Income Breeding in Male Ungulates: Causes and Consequences of Strategy Differences Among Species

“…Initially, most of the effort to understand both capital and income breeding and the differences between them was devoted to studying females at different phases of breeding from conception to egg laying, incubation and offspring-rearing in birds, and from conception to embryonic development, birth and lactation in mammals (Drent and Daan, 1980;Andersen et al, 2000;Boyd, 2000;Connan et al, 2019). Far fewer studies, however, considered males (but see Soulsbury, 2019), for which the contribution to reproduction is usually lower than for females. Despite this, reproduction may be demanding for males of some species, especially those -like ungulatescharacterized by high polygyny (Mysterud et al, 2004).…”