Compatibility drives female preference and reproductive success in the monogamous California mouse (Peromyscus californicus) more strongly than male testosterone measures

Abstract

Female assessment of male attractiveness and how preferred qualities impact reproductive success is central to the study of mate choice. Male attractiveness may depend on traits beneficial to the reproductive success (RS) of any female, termed ‘universal quality’, and/or on behavioral and biological interactions between potential mates that reflect ‘compatibility’. The steroid hormone testosterone (T) often underlies male attractiveness in rodents and is associated with enhanced paternal care in the monogamous and biparental California mouse (Peromyscus californicus). We hypothesized that (1) T-characteristics are universally attractive to female California mice and that (2) if reproductive success is higher for females mated with preferred males, then females mated with males preferred by other females will also have higher reproductive success. Alternatively, we speculated that pair compatibility, based on emergent pair qualities, is important for a species with coordinated offspring care. We assessed individual T-characteristics in three ways: (1) T-response to GnRH challenges (2) baseline T-level and (3) T-response to a female. Testosterone-response did not predict female preference, but females spent more time investigating males with higher baseline T (accounting for only 9.6% of the variation in investigation time). None of the T-measures was associated with RS. Females paired with males they preferred produced litters more quickly and had higher RS than females paired with their non-preferred males. Naïve females who did not undergo preference tests had equivalent RS regardless of whether their mate was preferred or non-preferred by another female. These data suggest that higher male T elicits investigation, but female preference in the California mouse is more strongly linked with compatibility because individual preference was a better predictor of RS than any T measure.

Male fidelity expressed through rapid testosterone suppression of ultrasonic vocalizations to novel females in the monogamous California mouse

“…This positive relationship in vocal production between males and females is intriguing because it suggests that some degree of vocal coordination or responsiveness may be occurring, possibility as a means of compatibility assessment, which is known to influence reproductive success in this species (Gleason et al, 2012b). Interestingly, T administration altered the relationship of vocal responsiveness, but not in a classically expected direction, in that female and male vocal output was uncorrelated among T-treated, non-paired males.…”

Sexual Dimorphism in the Brain of the Monogamous California Mouse (Peromyscus californicus)

“…Males and females of this species form monogamous breeding pairs [Ribble 1991] and defend joint territories [Ribble and Salvioni 1990] which is unique among mammals as only 3% of mammals are considered to be monogamous [Carter et al 1995]. The relatively unique natural history of California mice has contributed to its emergence as an important species for studying many aspects of behavior including development [Bester-Meredith and Marler 2003; Frazier et al 2006], parental behavior [de Jong et al 2009; Lambert et al 2011], aggression [Fuxjager and Marler 2010; Silva et al 2010; Trainor et al 2010b], mating preferences [Gleason et al 2011], communication [Kalcounis-Rueppell et al 2010], and stress [Chauke et al 2011; Trainor et al 2010a; Trainor et al 2011]. Although immunostaining studies have compared the chemoarchitecture of male and female California mice, there has been little quantification of the size of nuclei within the social behavior network or mesolimbic dopamine system [but see Gubernick et al 1993].…”

Sexual Modulation of Testosterone: Insights for Humans from Across Species

“…In a follow-up study, the authors investigated whether female California mice might use males' ΔT as a signal to choose mates who provide better quality paternal care. Unexpectedly, males' ΔT did not predict either female preference or reproductive success; instead, results suggested that biological or behavioral compatibility of the pair might be a better predictor of reproductive success in this biparental species (Gleason et al 2012).…”