Abstract
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.
Highlights
High rates of extra‐pair matings leading to appreciable paternity losses are commonplace in many socially monogamous species (Cohas & Allainé, 2009; Griffith, Owens, & Thuman, 2002)
High rates of extra‐pair paternity imply that cuckolding could be a viable alternative route to fitness, and pair‐bonded males may experience selection favouring the pursuit of extra‐pair matings
Over the course of two field seasons, one from 22 September to 28 October 2015 and one from 4 to 20 April 2016, we identified V. moorii territories each containing an active nest within a study quadrat (~100 m × ~50 m, depth range: 1.7–12.1 m) in the south of Lake Tanganyika (8°42′29.4′′S, 31°07′18.0′′E)
Summary
High rates of extra‐pair matings leading to appreciable paternity losses are commonplace in many socially monogamous species (Cohas & Allainé, 2009; Griffith, Owens, & Thuman, 2002). While extra‐pair copulations are largely under female control in many bird species (Birkhead & Møller, 1993), in fishes, cuckoldry typically occurs due to male intrusions with females exerting relatively less control (but see Reichard, Le Comber, & Smith, 2007; Li, Takeyama, Jordan, & Kohda, 2015; Alonzo, Stiver, & Marsh‐Rollo, 2016) These factors taken together suggest that, in fishes, pair‐bonded socially monogamous males could be highly prolific cuckolders. This work has shown that territorial males of multiple species are plastic in their reproductive behaviours, engaging in conventional tactics (e.g., courtship and resource‐holding) alongside alternative tactics (e.g., cuckoldry) These males must carefully weigh the benefits of seeking extra‐pair fertilizations against the costs of leaving their current offspring temporarily vulnerable (Candolin & Vlieger, 2013). How much paternity do brood‐tending (i.e., pair‐bonded) males lose due to cuckoldry from other males? Second, do brood‐tending males employ cuckoldry tactics, and by doing so can they fully offset their paternity losses at home? Third, how does the reproductive output of unpaired males compare with that of brood‐tending males? Fourth, are all unpaired males reproductively capable, or do they comprise a mixture of reproductive and non‐reproductive individuals?
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