Relationships between male secondary sexual traits, physiological state and offspring viability in the three-spined stickleback

Abstract

Background Sexual signals produced by males play a central role in sexual selection, but the relationship between these traits and the quality of the bearer are often ambiguous. Secondary sexual traits may represent genetic quality of the bearer, resulting in positive relationships with physiological state, or may be costly to produce, showing trade-off with physiological state. A number of studies have explored the relationships between secondary sexual traits and other functional traits, but few have studied their fitness consequences. We studied the link between diverse physiological traits and both morphological and behavioural sexual traits and examined how their interplay influences offspring viability in the three-spined stickleback. Results Male sticklebacks showing nest building and courtship behaviour were smaller than those not investing in reproductive activities. There was no evidence that the expression of red nuptial colouration and the quality of courtship behaviour of males are positively related to their metabolic rates, swim ability, oxidative damage and mtDNA copy number. However, individuals showing larger red nuptial colour areas had higher levels of oxidative DNA damage in their sperm. Male courtship behaviour and aggressiveness, but not red colour area, were good predictors of offspring hatching and survival. Conclusions Our results suggest that, in our study population at the southern edge of the species’ distribution, sexual colouration of male sticklebacks was not a good indicator of their body state, but both courtship quality and aggressiveness during the courtship are reliable cues of their gamete quality, influencing the viability of their offspring. Thus, females that choose mates based on their courtship behaviour will have high fitness. In the study population, which represents a fast pace-of-life with high reproductive rate and short lifespan, sexual ornaments of males may not honestly signal their physiological and physical state because they invest at maximum in a single reproductive season despite high costs.

Genetic compatibility exceeds possible ‘good genes’ effects of sexual selection in lake char

“…Male yellowness never predicted offspring performance in the direction that would be expected from ‘good genes’ hypotheses of sexual selection. This is in line with recent findings on three-spined stickleback ( Gasterosteus aculeatus ) where male coloration could not be linked to offspring viability [46].…”

“…Male yellowness never predicted offspring performance in the direction that would be expected from 'good genes' hypotheses of sexual selection. This is in line with recent findings on three-spined stickleback (Gasterosteus aculeatus) where male coloration could not be linked to offspring viability [46]. Mating systems that are not based on resources, like those of salmonids, are a challenge to evolutionary biologists because female choice is expected to lead to increased offspring survival ('good genes') or increased attractiveness of sons [47].…”

Parental kinship coefficient but not paternal coloration predicts early offspring growth in lake char

“…We conclude that if females could choose their mate, they would profit most from avoiding genetic similarity while ignoring male coloration to achieve the highest genetic benefit from mate choice. Analogous negative effects of genetic similarity were recently demonstrated in an amphibian (Byrne et al 2021 ), and analogous non-significant effects of male coloration on offspring viability were recently reported for three-spined stickleback ( Gasterosteus aculeatus ) (Chiara et al 2022 ).…”

Does paternal care influence mate preference? Male and female mating behavior in Threespine Stickleback ecotypes that differ markedly in parental care

“…This increase in courtship could be a signal of male quality as has been suggested in other studies that have reported that courtship intensity could be a stronger signal of quality than the presence of eggs in a male's nest that act as a primer for males to court more (Jamieson & Colgan, 1989 ). Similarly, males who court more have relatively higher offspring survival rate after hatching as seen in a population from Spain (Chiara et al, 2022 ).…”

“…Common female stickleback may be more attracted to white males as common male stickleback cannot invest as much energy in courtship and nuptial colouration, as it can reduce energy reserves and decrease in egg survival as seen in a population of stickleback from California (von Hippel, 2000). However, other studies examining courtship and hatching success found that in common and 15-spine sticklebacks males who courted more had higher offspring hatch and/or survival rates (Chiara et al, 2022;Östlund & Ahnesjö, 1998) and were preferred by females (Östlund & Ahnesjö, 1998), but did not find an association between female preference or male parental ability and the size of male 15-spine sticklebacks (Östlund & Ahnesjö, 1998).…”