The Evolution of Bourgeois, Parasitic, and Cooperative Reproductive Behaviors in Fishes

Among vertebrate classes, fishes exhibit by far the greatest variability in competitive and cooperative behaviors in male reproduction. Scramble competition between reproductive males is one possibility. Another possibility occurs when resources, mates, or locations can be monopolized, in which case males may invest in primary access to fertilizations by adopting a "bourgeois” strategy, or they may employ alternative mating tactics to evade the reproductive monopoly of other males. Adaptations in morphology, physiology, and behavior to bourgeois and alternative phenotypes are highly divergent. Here I review the functional characteristics that differ between bourgeois and parasitic phenotypes, and discuss the variability of alternative reproductive tactics at the levels of plasticity, determination, and selection. Examples will illustrate the importance of ecology, and will suggest that variation in reproductive tactics is largely adaptive. Behavioral solutions to competition for mates and fertilizations often involve agonistic behavior and conflict, but also cooperation among competitors (e.g., when subordinate males pay a price to bourgeois males for gaining access to fertilizable eggs). Application of molecular genetic tools has helped to uncover intricate sexual and social relationships in various fish species, including species that display some of the most complex reproductive and social patterns known among the vertebrate

Multiple paternity in the cooperatively breeding fish Neolamprologus pulcher

In cooperative breeders, mature males may compete for fertilizations. In this study, we measured the degree of multiple paternity in a natural population of a cooperatively breeding fish. Neolamprologus pulcher (Perciformes: Cichlidae) is a highly social cichlid endemic to Lake Tanganyika. We used highly variable microsatellite loci to survey 12 groups with an average number of 10.6 brood care helpers per group and a total of 43 offspring (mean 3.6 per brood). In 11 of 12 groups, all young were assigned to the dominant female. The dominant male sired all offspring in three groups, part of the offspring in four groups, and in five groups, he had no paternity at all. In total, 44.2% of young were not fathered by the current male territory owner. Multiple paternity was found in 5 of 12 broods (41.7 %), with 8 of 35 young (22.9 %) being sired by males other than the respective territory owners. This is an exceptionally high rate of extra-pair paternity among cooperatively breeding vertebrates. Neither helpers present in these territories during collection nor neighbouring males were unequivocally assigned to have sired these extra-pair young. However, behavioural observations suggest that male helpers may have produced these young before being expelled from the territory in response to this reproductive parasitism. We discuss these results in the light of reproductive skew theory, cooperative breeding in vertebrates and alternative reproductive tactics in fis

Consistent cooperation in a cichlid fish is caused by maternal and developmental effects rather than heritable genetic variation.

This is the author accepted manuscript. The final version is available from Royal Society via the DOI in this record.Studies on the evolution of cooperative behaviour are typically confined to understanding its adaptive value. It is equally essential, however, to understand its potential to evolve, requiring knowledge about the phenotypic consistency and genetic basis of cooperative behaviour. While previous observational studies reported considerably high heritabilities of helping behaviour in cooperatively breeding vertebrates, experimental studies disentangling the relevant genetic and non-genetic components of cooperative behaviour are lacking. In a half-sibling breeding experiment, we investigated the repeatability and heritability of three major helping behaviours performed by subordinates of the cooperatively breeding fishNeolamprologus pulcherTo experimentally manipulate the amount of help needed in a territory, we raised the fish in two environments differing in egg predation risk. All three helping behaviours were significantly repeatable, but had very low heritabilities. The high within-individual consistencies were predominantly due to maternal and permanent environment effects. The perceived egg predation risk had no effect on helping, but social interactions significantly influenced helping propensities. Our results reveal that developmentally plastic adjustments of provided help to social context shape cooperative phenotypes, whereas heritable genetic variation plays a minor role.Funding was provided by the ‘ProDoc’ program of the Swiss National Science Foundation (SNF, projects PDFMP3_137196 and 31003A_156881 to B.T.), and the ‘120% support grant’ to C.K. of the University of Bern

Predators, reproductive parasites, and the persistence of poor males on leks

Lekking males are thought to face strong directional selection on secondary sexual traits. How variation in male traits can persist under these conditions remains problematic (the lek paradox). Here, we present several game-theoretic models that show that avoidance of costly and mobile predators, sneakers, or brood parasites (enemies) leads to variation in female choice. This can result in maintenance of variation in male quality. "Enemies” will congregate around higher quality males. Females must then trade-off the benefits of mating with high-quality males against the increased risk of enemies. At equilibrium, the models predict a positive correlation between the quality of a male and the proportions of both enemies and females visiting him. In the first model, we use this framework to predict the lowest quality male on the lek that will receive any matings. In the second model, we examine the influence of this female-enemy game on the maintenance of variation in male quality. Low-quality males are likely to persist when enemies are costly to females or occur at high density, and when there is some spatial structure on the lek, so that neighboring males are typically of similar quality. If enemies are more costly to males than to females, high-quality males may benefit from receiving fewer female visits. In the third model, we consider the special case when enemies are male reproductive parasites. These models illustrate the importance of considering the simultaneous decisions of multiple players in mate choice game

Computer animations of color markings reveal the function of visual threat signals in Neolamprologus pulcher

© The Author (2016). Visual signals, including changes in coloration and color patterns, are frequently used by animals to convey information. During contests, body coloration and its changes can be used to assess an opponent's state or motivation. Communication of aggressive propensity is particularly important in group-living animals with a stable dominance hierarchy, as the outcome of aggressive interactions determines the social rank of group members. Neolamprologus pulcher is a cooperatively breeding cichlid showing frequent within-group aggression. Both sexes exhibit two vertical black stripes on the operculum that vary naturally in shape and darkness. During frontal threat displays these patterns are actively exposed to the opponent, suggesting a signaling function. To investigate the role of operculum stripes during contests we manipulated their darkness in computer animated pictures of the fish. We recorded the responses in behavior and stripe darkness of test subjects to which these animated pictures were presented. Individuals with initially darker stripes were more aggressive against the animations and showed more operculum threat displays. Operculum stripes of test subjects became darker after exposure to an animation exhibiting a pale operculum than after exposure to a dark operculum animation, highlighting the role of the darkness of this color pattern in opponent assessment. We conclude that (i) the black stripes on the operculum of N. pulcher are a reliable signal of aggression and dominance, (ii) these markings play an important role in opponent assessment, and (iii) 2D computer animations are well suited to elicit biologically meaningful short-term aggressive responses in this widely used model system of social evolution

Predator-induced maternal effects determine adaptive antipredator behaviors via egg composition.

In high-risk environments with frequent predator encounters, efficient antipredator behavior is key to survival. Parental effects are a powerful mechanism to prepare offspring for coping with such environments, yet clear evidence for adaptive parental effects on offspring antipredator behaviors is missing. Rapid escape reflexes, or "C-start reflexes," are a key adaptation in fish and amphibians to escape predator strikes. We hypothesized that mothers living in high-risk environments might induce faster C-start reflexes in offspring by modifying egg composition. Here, we show that offspring of the cichlid fish Neolamprologus pulcher developed faster C-start reflexes and were more risk averse if their parents had been exposed to cues of their most dangerous natural predator during egg production. This effect was mediated by differences in egg composition. Eggs of predator-exposed mothers were heavier with higher net protein content, and the resulting offspring were heavier and had lower igf-1 gene expression than control offspring shortly after hatching. Thus, changes in egg composition can relay multiple putative pathways by which mothers can influence adaptive antipredator behaviors such as faster escape reflexes

Experimentally induced helper dispersal in colonially breeding cooperative cichlids

The ‘benefits of philopatry' hypothesis states that helpers in cooperatively breeding species derive higher benefits from remaining home, instead of dispersing and attempting to breed independently. We tested experimentally whether dispersal options influence dispersal propensity in the cooperatively breeding Lake Tanganyika cichlids Neolamprologus pulcher and N. savoryi. Cooperative groups of these fishes breed in densely packed colonies, surrounded by unoccupied, but apparently suitable breeding habitat. Breeding inside colonies and living in groups seems to benefit individuals, for example by early detection and deterrence of predators. We show that despite a slight preference of both species for habitat with a higher stone cover, 40% of the preferred habitat remained unoccupied. On average, the colonies contained a higher number of (1) predators of adults, juveniles and eggs, (2) shelter competitors, and (3) other species including potential food competitors, compared to the outside colony habitat. Apparently, habitat differences cannot explain why these cichlids breed in colonies. Accordingly, dispersal may not be limited by a lack of suitable breeding shelters, but by the relatively higher risk of establishing an outside- compared to a within-colony breeding territory. To test whether cichlids prefer within- to outside-colony breeding territories, we provided breeding shelters inside the colony and at the colony edge and studied helper dispersal. As expected, significantly more shelters were occupied within the colony compared to the edge. New breeding pairs with several helpers occupied these shelters. We conclude that although breeding habitat is plentiful outside the colonies, helpers delay dispersal to obtain a higher quality breeding position within the group or colony eventually, or they disperse in groups. Our results suggest that (1) group augmentation and Allee effects are generally important for dispersal decisions in cooperatively breeding cichlids, consistent with the ‘benefits of philopatry hypothesis', and (2) habitat saturation cannot fully explain delayed dispersal in these specie

Female mouthbrooders in control of pre- and postmating sexual selection

The fertilization mode determines which sex has greater control over the offspring's sires. With internal fertilization, females can strongly influence the chances of different males' ejaculates to fertilize their eggs by the postmating sexual selection process referred to as cryptic female choice. In contrast, when fertilization is external and multiple males compete in this process, the outcome of pre- and postmating sexual selection is largely determined by the competitive quality of males and their sperm. Intermediate modes of fertilization as found in mouthbrooding fishes might allow for a greater maternal influence on her offspring's sire. Here, we show that in the maternal mouthbrooder Ophthalmotilapia ventralis, females collect sperm from different males in their mouth, and males can successfully fertilize eggs even if the female did not lay eggs with them. In the field, 25 of 30 clutches had multiple sires, and the fertilization success was significantly biased toward particular males in most clutches. A mate choice experiment revealed that females prefer to spawn with males possessing strongly elongated pelvic fins, a conspicuous secondary sexual character of males in this cichlid. Additionally, the body length of males partly explained their success in sperm competition within the females' mouth, a factor without apparent influence on female choice of partners with which to lay eggs. Hence, successful sires are determined by a 2-step process that is largely under female control; females select which males to spawn with and from which males they collect additional ejaculates for the subsequent sperm competition in their mout