Seasonal variation in cuckoldry rates in the socially monogamous cichlid fish Variabilichromis moorii.

Mating patterns in animal populations can respond to environmental conditions and consequently vary across time. To examine this variation in nature, studies must include temporal replicates from the same population. Here, we report temporal variation in genetic parentage in the socially monogamous cichlid Variabilichromis moorii from Lake Tanganyika, using samples of broods and their brood-tending parents that were collected across five field trips from the same study population. The sampled broods were either spawned during the dry season (three field trips) or during the rainy season (two trips). In all seasons, we detected substantial rates of extra-pair paternity, which were ascribed to cuckoldry by bachelor males. Paternity shares of brood-tending males were consistently higher, and the numbers of sires per brood were consistently lower, in broods that were spawned in the dry seasons compared to broods from the rainy seasons. In contrast, the strength of size-assortative pairing in our V. moorii population did not vary temporally. Seasonal fluctuations in environmental conditions, such as water turbidity, are proposed as a mechanism behind variable cuckolder pressure. Our data demonstrate the utility of long-term monitoring to improve our understanding of animal mating patterns. Supplementary Information: The online version contains supplementary material available at 10.1007/s10750-022-05042-0.

Nest defense in the face of cuckoldry: evolutionary rather than facultative adaptation to chronic paternity loss.

BACKGROUND: Raising unrelated offspring is typically wasteful of parental resources and so individuals are expected to reduce or maintain low levels of parental effort when their parentage is low. This can involve facultative, flexible adjustments of parental care to cues of lost parentage in the current brood, stabilizing selection for a low level of paternal investment, or an evolutionary reduction in parental investment in response to chronically low parentage. RESULTS: We studied parental care in Variabilichromis moorii, a socially monogamous, biparental cichlid fish, whose mating system is characterized by frequent cuckoldry and whose primary form of parental care is offspring defense. We combine field observations with genetic parentage analyses to show that while both parents defend their nest against intruding con- and hetero-specifics, males and females may do so for different reasons. Males in the study group (30 breeding pairs) sired 0-100% (median 83%) of the fry in their nests. Males defended less against immediate threats to the offspring, and more against threats to their territories, which are essential for the males' future reproductive success. Males also showed no clear relationship between their share of defense and their paternity of the brood. Females, on the other hand, were related to nearly all the offspring under their care, and defended almost equally against all types of threats. CONCLUSION: Overall, males contributed less to defense than females and we suggest that this asymmetry is the result of an evolutionary response by males to chronically high paternity loss in this species. Although most males in the current study group achieved high parentage in their nests, the average paternity in V. moorii, sampled across multiple seasons, is only about 55%. We highlight the importance and complexity of studying nest defense as a form of parental care in systems where defense may serve not only to protect current offspring, but also to ensure future reproductive success by maintaining a territory.

Inclusive fitness benefits mitigate costs of cuckoldry to socially paired males.

BACKGROUND: In socially monogamous species, reproduction is not always confined to paired males and females. Extra-pair males commonly also reproduce with paired females, which is traditionally thought to be costly to the females' social partners. However, we suggest that when the relatedness between reproducing individuals is considered, cuckolded males can suffer lower fitness losses than otherwise expected, especially when the rate of cuckoldry is high. We combine theoretical modeling with a detailed genetic study on a socially monogamous wild fish, Variabilichromis moorii, which displays biparental care despite exceptionally high rates of extra-pair paternity. RESULTS: We measured the relatedness between all parties involved in V. moorii spawning events (i.e. between males and females in social pairs, females and their extra-pair partners, and paired males and their cuckolders), and we reveal that males are on average more related to their cuckolders than expected by chance. Queller-Goodnight estimates of relatedness between males and their cuckolders are on average r = 0.038 but can range up to r = 0.64. This also increases the relatedness between males and the extra-pair offspring under their care. These intriguing results are consistent with the predictions of our mathematical model, which shows that elevated relatedness between paired males and their cuckolders can be adaptive for both parties when competition for fertilizations is strong. CONCLUSIONS: Our results show how cuckoldry by relatives can offset males' direct fitness losses with inclusive fitness gains, which can be substantial in systems where males face almost certain paternity losses.

Brood-tending males in a biparental fish suffer high paternity losses but rarely cuckold.

Extra-pair paternity within socially monogamous mating systems is well studied in birds and mammals but rather neglected in other animal taxa. In fishes, social monogamy has evolved several times but few studies have investigated the extent to which pair-bonded male fish lose fertilizations to cuckolders and gain extra-pair fertilizations themselves. We address this gap and present genetic paternity data collected from a wild population of Variabilichromis moorii, a socially monogamous African cichlid with biparental care of offspring. We show that brood-tending, pair-bonded males suffer exceptionally high paternity losses, siring only 63% of the offspring produced by their female partners on average. The number of cuckolders per brood ranged up to nine and yet, surprisingly, brood-tending males in the population were rarely the culprits. Brood-tending males sired very few extra-pair offspring, despite breeding in close proximity to one another. While unpaired males were largely responsible for the cuckoldry, pair-bonded males still enjoyed higher fertilization success than individual unpaired males. We discuss these results in the context of ecological and phenotypic constraints on cuckoldry and the fitness payoffs of alternative male tactics. Our study provides new insights into how pair-bonded males handle the trade-off between securing within-pair and extra-pair reproduction.

Sex Ratio Bias Leads to the Evolution of Sex Role Reversal in Honey Locust Beetles.

The reversal of conventional sex roles was enigmatic to Darwin, who suggested that it may evolve when sex ratios are female biased [1]. Here we present direct evidence confirming Darwin's hypothesis. We investigated mating system evolution in a sex-role-reversed beetle (Megabruchidius dorsalis) using experimental evolution under manipulated sex ratios and food regimes. In female-biased populations, where reproductive competition among females was intensified, females evolved to be more attractive and the sex roles became more reversed. Interestingly, female-specific mating behavior evolved more rapidly than male-specific mating behavior. We show that sexual selection due to reproductive competition can be strong in females and can target much the same traits as in males of species with conventional mating systems. Our study highlights two central points: the role of ecology in directing sexual selection and the role that females play in mating system evolution.

A rigorous comparison of sexual selection indexes via simulations of diverse mating systems.

Sexual selection is a cornerstone of evolutionary theory, but measuring it has proved surprisingly difficult and controversial. Various proxy measures--e.g., the Bateman gradient and the opportunity for sexual selection--are widely used in empirical studies. However, we do not know how reliably these measures predict the strength of sexual selection across natural systems, and most perform poorly in theoretical worst-case scenarios. Here we provide a rigorous comparison of eight commonly used indexes of sexual selection. We simulated 500 biologically plausible mating systems, based on the templates of five well-studied species that cover a diverse range of reproductive life histories. We compared putative indexes to the actual strength of premating sexual selection, measured as the strength of selection on a simulated "mating trait." This method sidesteps a key weakness of empirical studies, which lack an appropriate yardstick against which proxy measures can be assessed. Our model predicts that, far from being useless, the best proxy measures reliably track the strength of sexual selection across biologically realistic scenarios. The maximum intensity of precopulatory sexual selection s'max (the Jones index) outperformed all other indexes and was highly correlated with the strength of sexual selection. In contrast, the Bateman gradient and the opportunity for sexual selection were poor predictors of sexual selection, despite their continuing popularity.

Homage to Bateman: sex roles predict sex differences in sexual selection.

Classic sex role theory predicts that sexual selection should be stronger in males in taxa showing conventional sex roles and stronger in females in role reversed mating systems. To test this very central prediction and to assess the utility of different measures of sexual selection, we estimated sexual selection in both sexes in four seed beetle species with divergent sex roles using a novel experimental design. We found that sexual selection was sizeable in females and the strength of sexual selection was similar in females and males in role-reversed species. Sexual selection was overall significantly stronger in males than in females and residual selection formed a substantial component of net selection in both sexes. Furthermore, sexual selection in females was stronger in role-reversed species compared to species with conventional sex roles. Variance-based measures of sexual selection (the Bateman gradient and selection opportunities) were better predictors of sexual dimorphism in reproductive behavior and morphology across species compared to trait-based measures (selection differentials). Our results highlight the importance of using assays that incorporate components of fitness manifested after mating. We suggest that the Bateman gradient is generally the most informative measure of the strength of sexual selection in comparisons across sexes and/or species.