Why do female mice mate with multiple males?

Abstract

Females often show multi-male mating (MMM), but the adaptive functions are unclear. We tested whether female house mice (Mus musculus musculus) show MMM when they can choose their mates without male coercion. We released 32 females into separate enclosures where they could choose to mate with two neighboring males that were restricted to their own territories. We also tested whether females increase MMM when the available males appeared unable to exclude intruders from their territories. To manipulate territorial intrusion, we introduced scent-marked tiles from the neighboring males into males' territories, or we rearranged tiles within males' own territories as a control. Each female was tested in treatment and control conditions and we conducted paternity analyses on the 57 litters produced. We found that 46 % of litters were multiply sired, indicating that multiple paternity is common when females can choose their mates. Intrusion did not increase multiple paternity, though multiple paternity was significantly greater in the first trial when the males were virgins compared to the second trial. Since virgin male mice are highly infanticidal, this finding is consistent with the infanticide avoidance hypothesis. We also found that multiple paternity was higher when competing males showed small differences in their amount of scent marking, suggesting that females reduce MMM when they can detect differences in males' quality. Finally, multiple paternity was associated with increased litter size but only in the intrusion treatment, which suggests that the effect of multiple paternity on offspring number is dependent on male–male interactions.

Female attraction to male scent and associative learning: the house mouse as a mammalian model

“…This may be an important factor in reducing the risk of infanticide (Hrdy, 1979), as males reduce infanticidal behaviour towards their mate's offspring after cohabitation and copulation (Elwood & Ostermeyer, 1984;McCarthy & Saal, 1986;Soroker & Terkel, 1988). However, female house mice typically range across several male territories and frequently mate multiply with neighbouring territory owners; in a survey of wild-caught mice, 23% of litters were sired by multiple males (Dean, Ardlie, & Nachman, 2006) while multiple mating can be even higher in high-density captive populations (Stockley, Bottell, & Hurst, 2013;Thonhauser, Raveh, Hettyey, Beissmann, & Penn, 2013). Thonhauser et al (2013) found more multiple paternity of litters when scent mark investment among males in the local population was more even, suggesting that females showed less discrimination to mate with one particular territory owner.…”

Female House Mice do not Differ in Their Exploratory Behaviour from Males

“…temperate vs. arctic areas) or density situation (see Ganem 2012; and references therein), populations of this species are generally divided into small, more or less isolated, demes consisting of one dominant male, several subordinate males and females with their offspring (Crowcroft 1955;Reimer & Petras 1967;van Zegeren & van Oortmerssen 1981;Singleton 1983;Latham & Mason 2004). The dominant male monopolizes females and sires most of their pups (DeFries & McClean 1970;Singleton & Hay 1983) although multiple paternity occurs in approximately a quarter of litters (Potts et al 1991;Montero et al 2013;Thonhauser et al 2013Thonhauser et al , 2014Auclair et al 2014). Females roam freely within (and to some extent also between) deme territories (Wolff 1985;Hurst 1990;Gerlach 1996).…”

Does multiple paternity influence offspring disease resistance?

“…Yet, when female house mice are allowed to select their mates, they often mate with multiple males. For example, when females can choose to mate between one or two males, behavioural observations indicate that all females mate multiply (Rolland et al ., ), and paternity analyses show that 29–46% of litters are multiply sired (Thonhauser et al ., , ; Manser et al ., ). Moreover, in wild populations of house mice, the frequency of multiple paternity ranges between 6% and 43% [mean 30%: M. musculus domesticus (Dean et al ., ; Firman & Simmons, ); M. musculus musculus (Thonhauser et al ., )].…”

“…Scent marking in mice is a secondary sexual trait that indicates male health and other aspects of quality (Kavaliers & Colwell, ; Penn et al ., ; Zala et al ., ). Interestingly, when female mice are able to select their mates, they are more likely to produce multiple‐sired litters when their potential mates show similar levels of scent marking, whereas they are more likely to produce single‐sired litters, fathered by the high‐marking male, when their available mates differ in their scent marking (Thonhauser et al ., , b). The relationship between female multiple mating and parentage is not known for house mice, but it was suggested that females mate multiply when they detect no difference in male quality, or alternatively females may generally mate multiply and single paternity may be due to sperm competition or cryptic female choice.…”

“…The aim of this study was to compare the disease resistance of single‐ versus multiple‐sired litters produced by female house mice ( M. musculus musculus ) that were allowed to choose to mate with either one or two males (Thonhauser et al ., ). We investigated how the resulting offspring were able to clear (infection resistance) and cope (infection tolerance) with an experimental infection of Salmonella enterica serovar Typhimurium.…”