Female coloration, egg carotenoids and reproductive success: gobies as a model system

Abstract: In two-spotted gobies (Gobiusculus flavescens), females develop an orange belly as they approach sexual maturity. Toward the end of the single breeding season, males become rare and females compete for spawnings. Nest-holding males then prefer females with more colourful bellies and this trait has been suggested to act as a female ornament. I found a positive relationship between belly coloration and the coloration of the underlying gonads. This shows that belly coloration honestly reflects egg pigmentation, mainly because the transparency of the abdominal skin allows other fish to see the gonads directly. The factors contributing to variation in the nuptial coloration of female G. flavescens was examined in a series of investigations (Paper I). When gonads matured they became more colourful while the abdominal skin became more transparent. This caused an increase in nuptial coloration as females approached maturity. However, there was considerable variation in belly coloration also among fully mature females. Mature females had more colourful bellies late in the breeding season, partly due to an increase in gonad carotenoid concentration but also due to a seasonal increase in skin coloration. Analyses of gonads from wild-caught female G. flavescens showed the three main carotenoids to be astaxanthin, idoxanthin and adonixanthin (34%, 23% and 21% of the total carotenoid concentration, respectively). Compared to females of the five other gobiid species found in the same area, G. flavescens had much more colourful bellies. The unique ornamentation of G. flavescens females was achieved by the concurrent exaggeration of all signal components: gonad coloration, skin coloration and skin transparency. To understand how gonad and skin pigmentation interact in the nuptial coloration of female G. flavescens, the role of skin chromatophores was examined in detail (Paper II). Noradrenaline caused aggregation of chromatophore pigment and was used to experimentally reduce the contribution of skin chromatophores to the nuptial coloration. Interestingly, the aggregation of skin pigment weakened the positive relationship between belly and gonad coloration, despite an increase in skin transparency. The results show that female G. flavescens have a potential to use skin chromatophores to rapidly alter their nuptial coloration, thereby affecting the efficacy with which information about gonad coloration is conveyed.   Carotenoid-based ornamentation has often been suggested to signal mate quality, and species with such ornaments have frequently been used in studies of sexual selection. Carotenoids can be beneficial to animals in various ways, especially during sensitive life stages such as embryonic development. However, empirical work has so far provided equivocal evidence of beneficial effects of carotenoids in vivo. Because males invest heavily in offspring during incubation, the evolution of the male mate preference can be explained if colourful females provide males with eggs of higher quality. This hypothesis was tested by letting males spawn with naturally ‘colourful’ and ‘drab’ females, and comparing several reproductive parameters (Paper III).    Colourful females produced slightly larger clutches and eggs with significantly higher concentrations of total carotenoids than drab females, but their clutches were not of higher quality. In addition, there were no significant relationships between egg carotenoids and clutch quality. These results call into question a link between female nuptial coloration and offspring quality. In a second study, females were given two diets, differing only in carotenoid concentration (Paper IV). Females given carotenoid- rich feed attained a stronger nuptial coloration, laid more carotenoid-rich eggs and were more likely to spawn. This group also produced larvae that had a stronger phototactic response, suggesting higher offspring quality. This result suggests a direct benefit for males that choose to mate with colourful females. Other measures of reproductive success commonly reported in the literature, such as fertilization rate, hatching success and offspring susceptibility to starvation, were not affected by maternal carotenoid supply.In this thesis I have established a link between female ornamentation and egg carotenoid concentration, as well as a relationship between egg carotenoid concentration and offspring quality. The work constitute a uniquely detailed description of factors affecting variation in a nuptial signal and in its different components, and relate these to current theory on signal evolution.