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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.
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Within a species natural and sexual selection mechanisms may push male and female body sizes in opposite directions and towards extreme levels (Parker 1992; Vollrath 1998; Schütz & Taborsky 2003, 2005; Schütz et al. 2006; Fairbairn, Blanckenhorn & Szekely 2007). Extreme sexual size dimorphisms (SSDs) may facilitate the evolution of alternative reproductive tactics (ARTs) within the larger sex, because surviving to maturity takes a long time and is hence unlikely, causing some individuals to benefit from maturing early and acting as reproductive parasites (Taborsky 2001). In consequence, an intrasexual dimorphism may evolve with bourgeois individuals adopting a capital breeding strategy based on accumulating reserves for reproduction, and parasitic individuals reproducing early by acting as opportunistic income breeders.
Among vertebrates, fish show the greatest variability of alternative reproductive tactics in the male sex (Taborsky 1994, 2008; Avise et al. 2002; Mank & Avise 2006). Usually, bourgeois males that attempt to monopolize females are exploited by conspecific male competitors parasitizing their reproductive investment. The crucial distinction between these ARTs is their fundamentally different reproductive effort. Energy expenditure caused by behavioural, morphological and physiological effort entails generally much higher costs on bourgeois than on parasitic males (Taborsky 1994, 2008). Bourgeois males invest either in direct defence of mates, in monopolizing resources for females, or in displaying traits that attract females because they signal male quality. Parasitic males exploit the reproductive investment of bourgeois males by attempting to fertilize eggs quickly (streaking) or inconspicuously (sneaking; Gross 1982; Taborsky 1997).
Adaptations of bourgeois and parasitic tactics to reproductive competition are usually divergent and often contrary to each other (Gross 1982; Taborsky 1997, 2008; Oliveira, Taborsky & Brockmann 2008). At the behavioural level, bourgeois males often attempt to monopolize reproduction by defending a territory or mating site, which provides females with shelter, food, or breeding substrate (Kuwamura 1986; Sato & Gashagaza 1997; Taborsky 2001). In contrast, reproductive parasites benefit from an inconspicuous or swift performance that is confined to the act of spawning (Gross 1982; reviewed in Taborsky 1994). Morphological investment of bourgeois males includes the acquisition of large body size, conspicuous signals such as gaudy colouration or body appendices, and the development of weapons that increase fighting potential, such as the hooknose in salmon (Tchernavin 1938; Jones 1959). In parasitic males, small rather than large body size often increases the fertilization potential, because small males are less conspicuous, more mobile and harder to pursue (Gross 1982). In contrast, large testis size is an adaptation of parasitic males to sperm competition reflecting high energetic investment. Parasitic males typically have larger testes in relation to their body size than bourgeois males (Gage, Stockley & Parker 1995; Awata et al. 2006), because they are subject to sperm competition to a much higher degree than bourgeois males (Parker 1990; Petersen & Warner 1998; Taborsky 1998, 2001; however, see Tomkins & Simmons 2002 for a cautionary note). Physiological investment of bourgeois males involves the production of hormones (Brantley, Wingfield & Bass 1993) and possibly pheromones (Jonge, Ruiter & Hurk 1989; Resink et al. 1989), and it is generally characterized by an increased energy expenditure caused by investment in mate acquisition and brood care. This may reduce growth or body condition and thereby limit the time bourgeois males can be reproductively active (Sato 1994). In contrast, allocation of energy towards sperm production is the main way in which parasitic males can raise fertilization probability (Parker 1990).
The way individuals compensate for the resource demands of reproduction is an important cause of life-history variation (Jonsson 1997; Koivula et al. 2003). Some organisms fuel their reproductive expenditure from energy gained earlier and stored prior to use (‘capital breeders’), whereas others fuel it by feeding when they are reproductively active (‘income breeders’, Bonnet, Bradshaw & Shine 1998; Bonnet et al. 2001). For example, many large mammals are capital breeders, where body weight fluctuates strongly with season and year and relates to reproductive success reciprocally (Festa-Bianchet, Gaillard & Jorgenson 1998). In contrast, small mammals have been considered typical income breeders (Koivula et al. 2003), where body weight varies on a much shorter time scale (Andersen et al. 2000).
In Lamprologus callipterus (see Fig. 1), a shell brooding cichlid from Lake Tanganyika, two very distinct male life histories co-exist within a population. Among all animals, this fish species shows the most extreme sexual size dimorphism (SSD) with males being bigger than females (Schütz & Taborsky 2000, 2005; Schütz et al. 2006), which may favour the evolution of ARTs (Taborsky 2001). Indeed, in L. callipterus the two alternative male morphs differ extremely in their body size, behaviour, and reproductive performance (Taborsky 2001; Sato et al. 2004). Bourgeois males, hereafter referred to as nest males, are on average more than 12 times heavier than females (Schütz & Taborsky 2000). They construct nests of empty snail shells and defend them against competitors (Sato 1994; Maan & Taborsky 2008). Females enter a shell in a nest for spawning and care for the brood within this shell by guarding and fanning eggs and larvae for 10–14 days. During this time males hold the territory which they cannot leave and they rarely feed. Due to condition decrease during territory maintenance, their time to hold a territory seems to be limited (Sato 1994). Before reaching the size at which males can compete for nests, they may behave as sneakers by entering a territory during spawning to fertilize eggs while the nest owner is inattentive. This tactic is opportunistic and transitional, and occurs typically before the switch to nest male behaviour (Taborsky 2001).
Figure 1. Lamprolugus callipterus nest male in spawning position over a snail shell containing an egg laying female.
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Males of the second life history pathway halt growth long before reaching female size (‘dwarf males’). They attempt to enter shells in which females are spawning by wriggling past them towards the tip of the shell, from where they attempt to fertilize the eggs (‘wriggling tactic’; Taborsky 1998, 2001; Sato et al. 2004). These dwarf males often move on their own or in small groups visiting different territories, where they may also sit and wait for opportunities of reproductive parasitism. They may occasionally sneak fertilisations, similar to medium sized sneaker males of the bourgeois type (‘mouthing tactic’; Sato et al. 2004). The bourgeois and dwarf male pathways are fixed for life and reflect a Mendelian genetic polymorphism (Wirtz 2008). Within a population, the two tactics are probably maintained by frequency dependent selection, causing both tactics to render equal payoffs at equilibrium (Gross 1996; Brockmann & Taborsky 2008).
The aim of this study was to unravel the reproductive trade-offs and the different reproductive investment strategies of nest males and dwarf males, i.e. individuals adopting alternative life history pathways. These males differ extremely in size, with dwarf males weighing on average only 2·5% of nest males (Sato et al. 2004), which greatly affects their potential to accumulate reserves for reproduction. Koivula et al. (2003) pointed out, that ‘it is necessary to study trade-offs in the wild, where individuals face both the ecological and physiological costs of reproduction’. By comparing the reproductive effort patterns between nest and dwarf males in the field we examined whether nest males are behaving as ‘capital breeders’ and dwarf males as ‘income breeders’. We hypothesized that due to the requirement to defend a nest site continuously during breeding and hence reduced feeding opportunities, nest males must store much more energy for reproduction than dwarf males, and that the time nest males can hold a territory is constrained by their condition decrease when fasting. We expect nest males to be limited also at the level of sperm production, as they have to fertilize each egg with a separate ejaculate in this species (Bachar 2002), and they often face sperm competition with ejaculates of parasitic males. Due to their small size and limited storage capacity, dwarf males should continue to feed during reproduction instead of living from reserves. Their main reproductive constraint might be a small absolute testis size due to their small body size, and limited access to females due to the nest males’ monopolization. In accordance with substantial differences in resource holding potential, we expect nest males to expend more time and effort in aggression than dwarf males.
To test these hypotheses, at the behavioural level we recorded time budgets to measure the time spent with reproductive activities and feeding, and with other activities. At the morphological level, we determined the patterns of energy allocation in somatic and gonadic growth. At the physiological level we searched for possible somatic and gonadic limitations in reproduction. We conducted a field experiment to estimate the rate of condition decrease during fasting in nest males in order to determine the limit for territory maintenance as caused by feeding restrictions, and investigated sperm allocation of nest males in a lab experiment. For dwarf males, we determined how often they are able to dart into a nest during spawning of the nest males in the field.
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Our data show that the reproductive investment differs substantially between the two male morphs of L. callipterus. Behavioural time budgets in the field revealed that both, nest and dwarf males were active for about one third of their time. Nest males invested a lot in courtship behaviour, which was never displayed by dwarf males. In contrast, dwarf males fed for about 20% of the time during their reproductively active period, while bourgeois males largely starved during their entire nest holding periods. Dwarf males exhibited significantly less aggression than nest males. Aggressive behaviour was shown to raise the routine metabolic rate about four-fold in a closely related cichlid (Neolamprologus pulcher; Grantner & Taborsky 1998), so apparently nest males bear substantial behavioural energy costs compared to dwarf males, independent of the spawning process itself. Also in the European wrasse Symphodus ocellatus, with four types of male alternative reproductive behaviour, satellites never participate in nest building, courtship, direct brood care or interspecific defence (Taborsky, Hudde & Wirtz 1987), even though they cooperate with nest males in defence against other reproductive parasites. This resembles the patterns in other fish taxa like sunfishes (Dominey 1980; Gross 1982) and the Azorean rock-pool blenny (Oliveira et al. 2002).
Nest males showed a higher gonad free condition factor (GFCF) than dwarf males, which indicates their greater body reserves. Apparently, nest males need to store reserves for defending and maintaining a territory, as during their territory holding period they cannot leave the nest to feed. Therefore nest males acquire resources for reproduction in advance and use stored energy for reproduction, which is characteristic for ‘capital breeders’ (Houston et al. 2007). The amount of stored resources determines the nest holding period of bourgeois males, which was found to correlate positively with male size (Sato 1994).
Dwarf males had a nearly five times higher gonado-somatic index (1·73%) than nest males (0·36%; see also Sato et al. 2004; Schütz et al. 2006), which seems to suggest that they invest relatively more in gonads than nest males do. The slopes of testis allometry did not differ significantly between the two male tactics, and were considerably smaller than those of all 23 fish species from 11 families listed by Stoltz, Neff & Olden (2005). This suggests that in L. callipterus males, small body size is strongly compensated by high investment in testes, which renders relatively large testes in small individuals, regardless of their reproductive tactic. Interestingly, despite the highly significant difference in GSI between nest and dwarf males, our ancova analysis revealed no significant effect of tactic on testes size, but only a significant body size effect. Nest and dwarf males may compensate with higher gonadal investment for small body size for different reasons, however. For nest males, the crucial limit might be the enormous number of ejaculations (>200) required to fertilize a clutch of one female. For dwarf males, it is probably the intense sperm competition with nest males, which affects virtually 100% of their fertilization attempts.
In addition to the risk of sperm competition, another requirement should affect energy allocation of dwarf males. A fat body (i.e. high condition factor) may be disadvantageous when trying to enter a shell to wriggle past a spawning female (Sato et al. 2004). Therefore, dwarf males appear to behave optimally by using resources acquired for reproduction straight away after uptake, instead of using stored energy, which is typical for ‘income breeders’. Capital and income breeding are the ends of a continuum, and some species mix the two modes (Stearns 1992). Poeciliid fishes show the full spectrum from capital breeders such as guppies (Poecilia) and swordtails (Xiphophorus), to income breeders such as the least killifish, Heterandrai Formosa (Stearns 1992). Also in mammals, there might be a continuum from large species often performing as capital breeders, to small species rather acting as income breeders (Sandell 1989; Festa-Bianchet, Gaillard & Jorgenson 1998; Gould, Sussman & Sauther 2003). Most insects, such as butterflies, are essentially ‘capital breeders’, because nutrients acquired during the larval stage are stored and subsequently used for egg production during adulthood (Bergstrom & Wiklund 2002). So far, the concepts of capital and income breeding have been mainly used to discriminate between different tactics of resource use between species (Festa-Bianchet, Gaillard & Jorgenson 1998; Poizat, Rosecchi & Crivelli 1999; Boyd 2000; Gregory 2006; Ely et al. 2007), but a few studies have shown that this distinction is also useful in the intraspecific context. For example, most snakes are capital breeders (Bonnet et al. 1999), but reproducing female vipers may combine energy from ‘capital’ and ‘income’ to maximize their litter sizes in the face of fluctuating levels of prey abundance (Lourdais et al. 2003). Depending on food availability, the lizard C. versicolor adopts a strategy of capital breeding for production of the first clutch of their season, switching to income breeding later in the season when food becomes more abundant (Shanbhag 2003). We argue that capital and income breeding are also very useful concepts to discriminate between tactics within a species and within one sex.
Also the physiological limitations in reproduction appear to differ between nest and dwarf male L. callipterus. For nest males, the decrease in somatic condition with increasing time of holding a territory apparently limits their reproductive period. Our condition decrease experiment suggested that nest males could hold a territory for an average period of 103 days, if they were only food limited and had no additional costs of maintaining a territory and reproducing. However, the observed average nest holding period was only 33 days, which suggests that the energetic costs of territory maintenance and reproduction exceeded the opportunity costs entailed by restricted feeding more than two-fold. Sato (1994) found that in a northern population, larger males had longer territory holding periods than smaller males. In our field cage experiment, large males showed a higher condition decrease per day than small males, which was probably caused by the fact that all males, regardless of size, had the same limited space for feeding (i.e. 1 m2, corresponding to the natural territory size), which affected small males less severely than large males. However, large males can accumulate more reserves before founding a territory and they may use energy more efficiently than small males during reproduction, in other words they are more efficient capital breeders. When nest males abandon their territory they roam about outside the nesting area to feed, mostly in conspecific shoals (own obs.). The age distribution of nest owners indicates that multiple nesting periods are possible (Ripmeester 2004), but because of time limitations in our field season we were unable to determine interval lengths between two nesting periods of the same male.
Sperm shortage is another limitation for nest male reproduction. In our lab experiments spawning activity of L. callipterus nest males began to decrease after 3 h and dropped sharply after 5 h, even though the spawning of a clutch lasted much longer. L. callipterus females lay eggs one by one, so that each egg requires a separate ejaculation (Bachar 2002). Nest males may not be able to anticipate the duration of egg laying by the female. They can only control the number of sperm per ejaculation, but not the number of ejaculations required, which depends on the number of eggs laid and is hence under female control. Therefore, males may run out of sperm during a spawning, which may be more severe even with intense sperm competition in a natural setting.
In contrast, dwarf males appear to be limited primarily by the difficulty to enter a shell and wriggle past a spawning female. Nest males defend their nests very effectively, and the success of dwarf males largely depends on the temporary absence of large males (Sato et al. 2004). Combining Sato et al.’s (2004) and our results of nest male removal experiments during spawning in the field, in 42·0% of all cases (150 of 357) a dwarf male subsequently entered the nest. In 113 cases the mating behaviour of the dwarf male could be identified: in 71·7% (N = 81) dwarf males tried to wriggle into a shell or showed a variation of wriggling behaviour, and in 28·3% (N = 32) they showed mouthing behaviour similar to the spawning behaviour of nest males. Compared to these observations, in undisturbed situations, we observed mouthing and successful intrusions into a shell by wriggling each only twice in about 25 h of focal dwarf male observations (see also Sato et al. 2004). The comparison of undisturbed observations with experimental removal periods strongly suggests that dwarf males are ready to spawn when they stay near nests, but that they are usually prevented from entering shells or fertilizing eggs by the respective nest owners. Sato et al. (2004) found that wriggling was most likely successful when the respective dwarf male was small, and when small females were spawning in relatively large shells. The largest dwarf males may be unable to wriggle past a spawning female, because they never adopted wriggling but only performed mouthing and sperm release similar to medium sized sneaker males (Sato et al. 2004).
Our study showed that nest males differ from dwarf males in several behavioural, morphological, and physiological traits concerning reproductive investment and limitations in reproduction. We conclude that nest males usually bear much higher costs than dwarf males, and that nest males conform to the pattern of ‘capital breeders’, whereas dwarf males are typical ‘income breeders’. We should like to stress that capital breeding may not be the default for bourgeois male tactics in general. When nutritional resources contained in a reproductive territory suffice for the owner’s energy maintenance, for example, bourgeois males may be selected to perform as income breeders. Likewise, parasitic males may be selected to accumulate reserves and act as capital breeders, for instance when performing a sit-and-wait tactic at or within bourgeois males’ territories. This is indeed a rare behaviour performed by L. callipterus dwarf males (Sato et al. 2004), and its rarity might relate to the opposing selection pressure to keep their bodies small and slender to enable them to enter a shell during spawning. In L. callipterus the reproductive limitations of alternative male types diverge extremely due to their very different spawning performance, which illustrates the effects of disruptive selection in a species with alternative reproductive tactics at the levels of body size, behaviour, somatic and gonadic morphology, and physiology.