Coping with cuckoldry

Cuckoldry and alloparental care are widespread among animals, but their effects on the fitness of the involved parties are unclear in many instances. The question remains why males of so many species lack effective defenses against cuckoldry. The project will empirically examine factors that can mitigate the fitness consequences of being cuckolded and thus contribute to our understanding of what superficially appears as maladaptive behavior. Previous studies of cuckoldry have assumed high costs to the cuckolded male. Here, I include a new approach and question whether the costs incurred by high rates of cuckoldry are indeed as high as the number of foreign offspring in a males nest would suggest. Possibilities investigated here are: (1) Indirect fitness benefits reduce the costs suffered by cuckoldry, because parenting males are related to cuckolders or to their female mates. (2) Cuckolded males are themselves the cuckolders of other males. (3) Males reduce their paternal investment in response to cuckoldry. The study will be carried out in the cichlid fish Variabilichromis moorii. The breeding behavior of this species combines social monogamy, biparental care, low brood care investment, large brood sizes, and high and variable rates of multiple paternity. This combination differs from the hitherto studied typical avian and piscine breeding systems, and requires novel solutions to the problem of cuckoldry. Importantly, a so far neglected factor - indirect fitness for cuckolded males - is addressed. The project includes extensive field work and sampling at Lake Tanganyika in Zambia to assess paternity, quantify brood care investment and identify the cuckolding males; comprehensive genetic analyses to reconstruct paternity and relatedness; and laboratory experiments to test male responses to manipulations of their share in paternity, and biases in mate preferences and male- male aggression for or against relatives. Within a study quadrat, the positions of all territorials will be mapped and tissue samples for DNA analysis will be taken from adults and broods. Brood care investment will be quantified in nests within the quadrat, and paternity of the caring males will be determined by microsatellite DNA analyses. Microsatellite profiles will also identify the cuckolding males, e.g. if cuckolders are nearby territorials. Test for elevated relatedness between pair members, and between breeding males and their cuckolders, will inform on potential inclusive fitness gains. Tests for spatial aggregations of relatives will demonstrate whether mating and cuckolding among kin should there be evidence for this follows from preferences for relatives or from the kin structure in the population. Finally, laboratory experiments will test whether males decrease their brood care efforts in response to a reduction in their paternity, pair preferentially with related females and bias aggression towards unrelated males.

In many animals, notably songbirds and some fish, brood care is provided by the parent pair. Fish parents defend against numerous brood predators threatening to intrude into the breeding territory. Despite being socially paired, the male partner is often not the father of all young in the brood - rather, cuckolding males fertilized some of his female mate's offspring. This means that the nest-tending males not only lose a proportion of their potential reproductive success to the cuckolders, but they also invest brood care into foreign young. This project investigated factors hypothesized to mitigate the costs incurred by cuckoldry. Conducting field observations and experiments in the African Lake Tanganyika as well as comprehensive genetic relatedness analysis, we tested whether nest-tending males of the cichlid fish Variabilichromis moorii balance paternity losses suffered in their own nests with reproduction in other nests (no, they don't), whether they adjust their brood care investment to their paternity share in the current brood (no, they don't either), and finally, whether they are related to their cuckolders. The latter hypothesis was confirmed: average relatedness between nest-tending males and their cuckolders was slightly higher than expected for chance combinations. This entails a low level of relatedness between the nest-tending males and the foreign young. Although low indeed, from an evolutionary perspective this relatedness improves the situation for the cuckolded males compared to losing paternity to unrelated males. Our study provided the first empirical evidence for a role of relatedness in the distribution of reproductive success between paired nest-holders and cuckolders. Overall, the rate of cuckoldry across several field seasons was high: average paternity shares of nest-tending males were 50%, and ranged from 0-100%. While the males' defence activities on a given nest were not correlated with their paternity share in that nest, males contributed less to defence against brood predators than their female partners overall. Nest-tending females were typically the genetic mothers of the entire brood. Therefore, broods are on average more valuable to females than to their male partners, and this asymmetry is reflected in the division of brood defence between them. After experimentally removing one partner for several days from the nest, females defended their brood successfully, whereas many of the males lost their brood quickly. In contrast to the asymmetries in defence against brood predators, males and females contributed equally to defence against territory competitors. Although male territory defence of course benefits the brood in the territory, our results suggest that male behavior which is - at first glance - interpreted as brood care, may in fact be driven by other motives such as protection of the territory. This may explain the persistence of this behavior in the face of chronically high paternity loss.