The social circuitry of the mammalian brain can impact an animal's physiology, behavior, neurochemistry, and neuroanatomy from both evolutionary and life-history perspectives (Blumenthal and Young, 2023; Ferreira-Fernandes and Peça, 2022; Lukas and Clutton-Brock, 2013; Nelson, 2015; van der Horst and Maree, 2014). In the mammalian reproductive system, mating strategies and the prevalence of sexual promiscuity in a species often correlate to trends in reproductive physiology (Kramer and Russell, 2015; Lukas and Clutton-Brock, 2013; Ophir and delBarco-Trillo, 2007; Schacht and Kramer, 2019; van der Horst and Maree, 2014). For example, there is an evolutionary pattern among male mammals that differences in testis size relative to body mass between species serve as an indicator of general female promiscuity in the species, with low rates of sperm competition resulting in smaller testes relative to body size (Kramer and Russell, 2015; Schacht and Kramer, 2019; van der Horst and Maree, 2014). From an individual, life history perspective, social encounters and the extrinsic social environment can impact gonad function via the hypothalamic-gonadal-pituitary (HPG) axis (Carter, 1987; Carter et al., 1980; Dixson and Anderson, 2004; Firman et al., 2018; Koyama and Kamimura, 2000; Lukas and Clutton-Brock, 2013; Maruska and Fernald, 2011; Ramm and Stockley, 2009a; Taylor et al., 1986). One common example of this phenomenon in females is the presence of induced ovulation in many species (Carter et al., 1980; Dal Bosco et al., 2011; Larivière and Ferguson, 2003). In males, this often manifest as impacts on testicular function and/or sperm quality (Dixson and Anderson, 2004; Firman et al., 2018; Koyama and Kamimura, 2000; Lukas and Clutton-Brock, 2013; Maruska and Fernald, 2011; Ramm and Stockley, 2009a). Social triggers of these changes often involve male-male competition (Maruska and Fernald, 2011; Ramm and Stockley, 2009a), but may also include things such as sexual experience (Taylor et al., 1986) and parental status (Bales and Saltzman, 2016; Reburn and Wynne-Edwards, 1999).

Most work investigating the impacts of the social environment on male reproductive function in mammals has been done in promiscuous, non-paternal species. Little investigation has been done on this topic in socially monogamous mammals, which make up ∼5–9 % of the class (Blumenthal and Young, 2023; Lukas and Clutton-Brock, 2013; van der Horst and Maree, 2014). While paternal care is rare in mammals, it occurs in 56–59 % of socially monogamous species (Lukas and Clutton-Brock, 2013; Stockley and Hobson, 2016). Social monogamy is sometimes erroneously correlated with sexual fidelity, which does not reflect the true nature of many socially monogamous species that frequently exhibit variable rates of extra-pair sexual encounters (EPCs) (Lambert et al., 2018; Ophir et al., 2008; Young, 2003). The presence of both a socially monogamous, biparental mating style as well as variable sperm competition creates an intriguing situation regarding male reproductive function and plasticity. Social monogamy provides reliable access to a sexual partner (Lambert et al., 2018) and paternal care can increase reproductive success (Stockley and Hobson, 2016). However, parenting offspring that may not be one's own due to EPCs is costly from a fitness perspective. This generates a need for paired males to reconcile the convenience of a consistent sexual partner while also reducing the likelihood of raising offspring that are not their own.

Prairie voles (Microtus ochrogaster) – a hamster-sized, burrowing rodent native to North American prairies – may serve as an excellent model species for investigating the impacts of the social environment on male reproductive function in socially monogamous, biparental mammals (Young, 2003). In addition to being socially monogamous, prairie vole males are highly paternal (Getz et al., 1981; McGraw and Young, 2010) and even alloparental (Finton et al., 2022; Roberts et al., 1998). Female prairie voles exhibit social modulation of their reproductive organs and behavior. They are induced ovulators and will remain in an anestrus state until exposed to an unfamiliar conspecific male or one's urine (Carter, 1987; Carter et al., 1980). They also exhibit a direct familial barrier to reproduction and will not normally ovulate when exposed only to their fathers and male littermates (Carter et al., 1980). On the contrary, no investigation has been done to determine the effect of novel female exposure in male prairie voles. In general, little is known about how the social environment affects testicular function in male prairie voles and how those effects may be specifically related to the prevalence of social monogamy and paternal care exhibited by the species. Prairie voles offer the opportunity to study the relationship between mating and parental strategies and male reproductive physiology in a controlled, laboratory setting.

To elucidate the relationship between novel female exposure and testicular plasticity with respect to species and broader species mating strategies, we will compare the effects of novel female exposure on testicular function in three rodent species – the socially monogamous and biparental North American prairie vole, the closely related promiscuous North American meadow vole (Microtus pennsylvanicus), and the distantly related promiscuous house mouse (Mus musculus).

Sperm competition can alter reproductive function in rodents, including house mice and meadow voles (delBarco-Trillo and Ferkin, 2006; Firman et al., 2018; Ramm and Stockley, 2009a). To our knowledge, the effects of sperm competition on prairie vole reproductive function have never been directly investigated. Because house mice and meadow voles do not form pair bonds nor provide paternal care, we hypothesize that novel female exposure alone in the absence of male competition will not induce any changes in testis size, sperm counts, or testicle histology in these species. In contrast, we hypothesize that male prairie voles will exhibit an increase in testis size and sperm production solely in response to female exposure due to the reproductive pressures generated by social monogamy and paternal care.