1. Adopting alternative reproductive tactics may require divergent solutions to reproductive competition among individuals of a population. Often investment in reproduction differs substantially between individuals pursuing bourgeois and parasitic tactics, which may result in different trade-offs and limitations.
2. Here we identify divergent behavioural, morphological and physiological traits of bourgeois and parasitic male morphs in Lamprologus callipterus, a Lake Tanganyika cichlid with an extreme size dimorphism among males. We focus on limiting factors and compare these between large, nest-building males and dwarf males parasitizing their reproductive effort.
3. Only nest males invest in courtship, and they exhibit much more aggression than dwarf males. In contrast, dwarf males spend 20% of their time feeding, whereas nest males hardly ever feed.
4. Nest males accumulate reserves before breeding and use these up before taking a reproductive break, thereby performing a ‘capital breeder’ strategy. In contrast, dwarf males use assimilated energy immediately for reproduction, thus acting as ‘income breeders’. This is a requirement of their spawning tactic, which only works out with a small and slim body.
5. A field experiment showed that nest males lose weight by their restricted feeding opportunities while holding a nest, which would allow them to hold a territory for 103 days on average. Due to their reproductive investment, however, they held territories only for a mean period of 33 days, which reveals the relative importance of opportunity costs and reproductive expenditure.
6. Nest males are also limited by the requirement to fertilize each egg of a clutch with a separate ejaculate. Their ejaculation rate and the number of sperm released both decline sharply after 5 h, whereas undisturbed spawning lasts 2–4 h longer than that.
7. There is a strong allometric relationship between body mass and gonad weight, with smaller males of both tactics investing disproportionately more in testes than large males. The major limitation of dwarf males is apparently access to spawning females, which is prevented by the monopolization of nest owners and becomes more difficult with increasing size of dwarf males.
8. Our results show that different males in a population may act as capital or income breeders depending on tactic and may face very different limitations, which is a direct result of highly divergent spawning tactics and resulting body sizes.
9. We argue that capital and income breeding are useful concepts to understand divergent life history decisions associated with alternative reproductive tactics, i.e. behavioural polymorphisms within a species and within one sex. It might turn out that in general, bourgeois tactics rather adopt a capital breeding strategy whereas parasitic tactics are inclined to perform as income breeders, due to the diverging constraints faced by these types of reproduction, although we discuss possible exceptions.