Peter D. Dijkstra

Social stimulation, nuptial colouration, androgens and immunocompetence in a sexual dimorphic cichlid fish

The nature of the costs maintaining honesty of sexual signalling in inter- and intrasexual interactions remains a contentious issue. For carotenoid-based colour ornaments, it has been hypothesized that the honesty of the signal is enforced when carotenoid allocation to colour expression is traded off against carotenoid availability for immunocompetence. In addition, honesty is enforced if androgens required for colour expression are immunosuppressive. We tested whether there is a trade-off between colour expression and immunocompetence in a lek-breeding haplochromine cichlid fish, Pundamilia nyererei, from Lake Victoria with a carotenoid-based nuptial dress. First, we showed that expression of red nuptial colouration and social rank in a group were positively correlated. We then successfully manipulated the level of colour advertisement by socially stimulating individually housed males with a rival male: Stimulated males developed larger areas of red nuptial colouration and had higher levels of circulating 11-ketotestosterone (11-KT) than non-stimulated males. We subsequently tested the humoral immune response to a novel antigen (sheep red blood cells). There was no overall significant effect of social stimulation on antibody production, but in the stimulated males, the degree of red colouration and the antibody response were negatively correlated. This significant interaction between colour and treatment thus shows that the negative correlation between colouration and antibody production is dependent on the (manipulated) social environment. This study provides correlational and experimental evidence for a trade-off between expression of a sexual trait and one component of immune function in fish. We found no evidence for a direct effect of 11-KT on antibody production, and we discuss alternative mechanisms that could mediate the trade-off.

Can male-male competition stabilize speciation? A test in Lake Victoria haplochromine cichlid fish

It has been suggested that sympatric speciation can be driven by sexual selection on male mating traits alone. However, a fundamental problem for this process is the lack of ecological differentiation that would stabilize the coexistence of incipient species through frequency-dependent selection. Such selection can also occur if male aggression is primarily directed towards similar rather than towards dissimilar phenotypes, so that rare male phenotypes would enjoy a negatively frequency-dependent fitness advantage. We experimentally tested such an aggression bias in two recently diverged, ecologically and anatomically similar sympatric cichlid species pairs of the genus Pundamilia from Lake Victoria. Territorial males of a pair of partially reproductively isolated species with red and blue nuptial coloration, respectively, studied in the laboratory were confronted simultaneously with both colour types enclosed in transparent tubes. Red males were more aggressive to red stimuli under white light but not when colour differences were masked under green light. Blue males were equally aggressive to both stimuli in both light conditions. Males of two apparently fully reproductively isolated species, again one with red and one with blue nuptial coloration, studied in the field, both directed more aggressive behaviour towards conspecific than towards heterospecific stimulus males. The differential allocation of aggression would create an advantage for males of the less abundant phenotype or species, thereby potentially supporting stable coexistence of the phenotypes. The finding that this effect was less clear in the partially reproductively isolated species pair than in the fully isolated species pair is discussed.

Territory quality affects female preference in a Lake Victoria cichlid fish

Mate preferences on male colour have been implicated in generating and maintaining species diversity among haplochromine cichlid fish. Their lek-like mating system suggests that not only male colour but also territory quality is instrumental in mate choice. We assessed the relative importance of territory quality and male colour in mate choice by testing whether territory quality can override the female preference for males of her own colour in the Lake Victoria cichlid genus Pundamilia. First, we showed in experimental groups that the dominant male preferentially monopolised a large tube relative to a small tube. The situation mimics quality difference in rocky crevices that serves as a focal point for male courtship display. Second, in mate-choice tests, Pundamilia nyererei females were allowed to choose between closely related P. nyererei and P. pundamilia males; these species differ strikingly in male nuptial coloration, but little else. We gave either both males the same small tube or one of them a large tube. The preference of P. nyererei females for P. nyererei males in the control situation (where both males had a small tube) was significantly diminished in favour of P. pundamilia males when the latter had the large tube. The results provide experimental evidence that differences in territory quality can override the female preference for males of her own colour. This finding is critical for a recent hypothesis proposing that male competition for mating territories can facilitate the process of sympatric speciation by sexual selection.

'Winner effect' without winning : Unresolved social conflicts increase the probability of winning a subsequent contest in a cichlid fish

Previous winning experience increases the probability of winning a subsequent contest. However, it is not clear whether winning probability is affected only by the outcome of the contest (winning or losing) or whether fighting experience itself is also sufficient to induce this effect. We investigated this question in the East African cichlid fish Pundamilia spec. To create an unresolved conflict we allowed males to fight their own mirror image prior to a real fight against a size-matched non-mirror-stimulated control male. When males fight their own mirror image, the images response corresponds to the action of the focal animal, creating symmetrical fighting conditions without the experience of losing or winning. We found that mirror-stimulated males were more likely to win an ensuing contest than control males. Interestingly, in this species mirror stimulation also induced an increase in circulating androgens, which is consistent with the hypothesis that stimulation of these sex steroids during aggressive encounters may prepare the animal for subsequent encounters. Our results suggest that fighting experience alone coupled with an androgen response, increases the likelihood of winning, even in the absence of a winning experience.

The role of physiology in the divergence of two incipient cichlid species.

Sexual selection on male coloration has been implicated in the evolution of colourful species flocks of East African cichlid fish. During adaptive radiations, animals diverge in multiple phenotypic traits, but the role of physiology has received limited attention. Here, we report how divergence in physiology may contribute to the stable coexistence of two hybridizing incipient species of cichlid fish from Lake Victoria. Males of Pundamilia nyererei (males are red) tend to defeat those of Pundamilia pundamilia (males are blue), yet the two sibling species coexist in nature. It has been suggested that red males bear a physiological cost that might offset their dominance advantage. We tested the hypothesis that the two species differ in oxidative stress levels and immune function and that this difference is correlated with differences in circulating steroid levels. We manipulated the social context and found red males experienced significantly higher oxidative stress levels than blue males, but only in a territorial context when colour and aggression are maximally expressed. Red males exhibited greater aggression levels and lower humoral immune response than blue males, but no detectable difference in steroid levels. Red males appear to trade off increased aggressiveness with physiological costs, contributing to the coexistence of the two species. Correlated divergence in colour, behaviour and physiology might be widespread in the dramatically diverse cichlid radiations in East African lakes and may play a crucial role in the remarkably rapid speciation of these fish.

Male-Male Competition as a Force in Evolutionary Diversification: Evidence in Haplochromine Cichlid Fish

It has been suggested that intrasexual competition can be a source of negative frequency-dependent selection, causing agonistic character displacement and facilitating speciation and coexistence of (sibling) species. In this paper we synthesise the evidence that male-male and female-female competition contributes to cichlid diversification, showing that competition is stronger among same-coloured individuals than those with different colours. We argue that intrasexual selection is more complex because there are several examples where males do not bias aggression towards their own type. In addition, sibling species or colour morphs often show asymmetric dominance relationships. We briefly discuss potential mechanisms that might promote the maintenance of covariance between colour and aggression-related traits even in the face of gene-flow. We close by proposing several avenues for future studies that might shed more light on the role of intrasexual competition in cichlid diversification.

No effect of blue on winning contests in judo.

A study by Rowe et al. reported a winning bias for judo athletes wearing a blue outfit relative to those wearing a white one during the 2004 Olympics. It was suggested that blue is associated with a higher likelihood of winning through differential effects of colour on opponent visibility and/or an intimidating effect on the opponent. However, we argue that there is no colour effect on winning in judo. We show that alternative factors, namely allocation biases, asymmetries in prior experience and differences in recovery time are possible confounding factors in the analysis of Rowe et al. After controlling for these factors, we found no difference in blue and white wins. We further analysed contest outcomes of 71 other major judo tournaments and also found no winning bias. Our findings have implications for sports policy makers: they suggest that a white–blue outfit pairing ensures an equal level of play.

Frequency-Dependent Social Dominance in a Color Polymorphic Cichlid Fish

A mechanism commonly suggested to explain the persistence of color polymorphisms in animals is negative frequency‐dependent selection. It could result from a social dominance advantage to rare morphs. We tested for this in males of red and blue color morphs of the Lake Victoria cichlid, Pundamilia. Earlier work has shown that males preferentially attack the males of their own morph, while red males are more likely to win dyadic contests with blue males. In order to study the potential contribution of both factors to the morph co‐existence, we manipulated the proportion of red and blue males in experimental assemblages and studied its effect on social dominance. We then tried to disentangle the effects of the own‐morph attack bias and social dominance of red using simulations. In the experiment, we found that red males were indeed socially dominant to the blue ones, but only when rare. However, blue males were not socially dominant when rare. The simulation results suggest that an own‐morph attack bias reduces the social dominance of red males when they are more abundant. Thus, there is no evidence of symmetric negative frequency‐dependent selection acting on social dominance, suggesting that additional fitness costs to the red morph must explain their co‐existence.

Complex structural and regulatory evolution of the pro-opiomelanocortin gene family

The melanocortin system is a neuroendocrine machinery that has been associated with phenotypic diversification in a number of vertebrate lineages. Central to the highly pleiotropic melanocortin system is the pro-opiomelanocortin (pomc) gene family, a family of pre-prohormones that each give rise to melanocyte stimulating hormone (MSH), adrenocorticotropic releasing hormone (ACTH), β-lipotropin hormone, and β-endorphin. Here we examine the structure, tissue expression profile, and pattern of cis transcriptional regulation of the three pomc paralogs (α1, α2, and β) in the model cichlid fish Astatotilapia burtoni and other cichlids, teleosts, and mammals. We found that the hormone-encoding regions of pomc α1, pomc α2 and pomc β are highly conserved, with a few notable exceptions. Surprisingly, the pomc β gene of cichlids and pomacentrids (damselfish) encodes a novel melanocortin peptide, ε-MSH, as a result of a tandem duplication of the segment encoding ACTH. All three genes are expressed in the brain and peripheral tissues, but pomc α1 and α2 show a more spatially restricted expression profile than pomc β. In addition, the promoters of each pomc gene have diverged in nucleotide sequence, which may have facilitated the diverse tissue-specific expression profiles of these paralogs across species. Increased understanding of the mechanisms regulating pomc gene expression will be invaluable to the study of pomc in the context of phenotypic evolution.

Intrasexual competition among females and the stabilization of a conspicuous colour polymorphism in a Lake Victoria cichlid fish

The maintenance of colour polymorphisms within populations has been a long-standing interest in evolutionary ecology. African cichlid fish contain some of the most striking known cases of this phenomenon. Intrasexual selection can be negative frequency dependent when males bias aggression towards phenotypically similar rivals, stabilizing male colour polymorphisms. We propose that where females are territorial and competitive, aggression biases in females may also promote coexistence of female morphs. We studied a polymorphic population of the cichlid fish Neochromis omnicaeruleus from Lake Victoria, in which three distinct female colour morphs coexist: one plain brown and two blotched morphs. Using simulated intruder choice tests in the laboratory, we show that wild-caught females of each morph bias aggression towards females of their own morph, suggesting that females of all three morphs may have an advantage when their morph is locally the least abundant. This mechanism may contribute to the establishment and stabilization of colour polymorphisms. Next, by crossing the morphs, we generated sisters belonging to different colour morphs. We find no sign of aggression bias in these sisters, making pleiotropy unlikely to explain the association between colour and aggression bias in wild fish, which is maintained in the face of gene flow. We conclude that female–female aggression may be one important force for stabilizing colour polymorphism in cichlid fish.