Long-Term Effects of Fatherhood on Morphology, Energetics, and Exercise Performance in California Mice (Peromyscus californicus).

In male mammals that provide care for their offspring, fatherhood can lead to changes in behavioral, morphological, and physiological traits, some of which might constitute trade-offs. However, relatively little is known about these changes, especially across multiple reproductive bouts, which are expected to magnify differences between fathers and nonreproductive males. We evaluated consequences of fatherhood in the monogamous, biparental California mouse (Peromsycus californicus) across seven consecutive reproductive bouts. We compared breeding adult males (housed with sham-ovariectomized females) with two control groups: nonbreeding males (housed with ovariectomized females treated with estrogen and progesterone to induce estrous behavior) and virgin males (housed with untreated ovariectomized females). At five time points (before pairing, early postpartum of the first litter, late postpartum of the second litter, early postpartum of the sixth litter, and late postpartum of the seventh litter or comparable time points for nonbreeding and virgin males), we measured males' body composition, hematocrit, predatory aggression, resting metabolic rate, maximal oxygen consumption (V˙O2 max⁡), grip strength, and sprint speed. We also weighed organs at the final time point. We predicted that fathers would have lower relative body fat and lower performance abilities compared with control groups and that these effects would become more pronounced with increasing parity. Contrary to predictions, breeding and control males differed in surprisingly few measures, and the number and magnitude of differences did not increase with parity. Thus, our expectations regarding trade-offs were not met. As reported in studies of single reproductive events, these results suggest that fatherhood has few costs in this species when housed under standard laboratory conditions, even across multiple reproductive bouts.

Effects of short- and long-term cold acclimation on morphology, physiology, and exercise performance of California mice (Peromyscus californicus): potential modulation by fatherhood.

California mice (Peromyscus californicus) differ from most other mammals in that they are biparental, genetically monogamous, and (compared with other Peromyscus) relatively large. We evaluated effects of cold acclimation on metabolic rate, exercise performance, and morphology of pair-housed male California mice, as well as modulation of these effects by fatherhood. In Experiment 1, virgin males housed at 5° or 10 °C for approximately 25 days were compared with virgins housed at standard vivarium temperature of 22 °C. Measures included resting metabolic rate (RMR), maximal oxygen consumption ([Formula: see text]max), grip strength, and sprint speed. In Experiment 2, virgin males housed at 22 °C were compared with three groups of males housed at 10 °C: virgins, breeding males (housed with a female and their pups), and non-breeding males (housed with an ovariectomized, estrogen- and progesterone-treated female) after long-term acclimation (mean 243 days). Measures in this experiment included basal metabolic rate (BMR), [Formula: see text]max, maximal thermogenic capacity ([Formula: see text]sum), and morphological traits. In Experiment 1, virgin males housed at 5° and 10 °C had higher RMR and [Formula: see text]max than those at 22 °C. In Experiment 2, 10 °C-acclimated groups had shorter bodies; increased body, fat, and lean masses; higher BMR and [Formula: see text]sum, and generally greater morphometric measures and organ masses than virgin males at 22 °C. Among the groups housed at 10 °C, breeding males had higher BMR and lower [Formula: see text]max than non-breeding and/or virgin males. Overall, we found that effects of fatherhood during cold acclimation were inconsistent, and that several aspects of cold acclimation differ substantially between California mice and other small mammals.

Effects of a physical and energetic challenge on male California mice (Peromyscus californicus): modulation by reproductive condition.

Reproduction strongly influences metabolism, morphology and behavior in female mammals. In species in which males provide parental care, reproduction might have similar effects on fathers. We examined effects of an environmental challenge on metabolically important physiological, morphological and behavioral measures, and determined whether these effects differed between reproductive and non-reproductive males in the biparental California mouse (Peromyscus californicus). Males were paired with an ovary-intact female, an ovariectomized female treated with estrogen and progesterone to induce estrus, or an untreated ovariectomized female. Within each group, half of the animals were housed under standard laboratory conditions and half in cages requiring them to climb wire towers to obtain food and water; these latter animals were also fasted for 24 h every third day. We predicted that few differences would be observed between fathers and non-reproductive males under standard conditions, but that fathers would be in poorer condition than non-reproductive males under challenging conditions. Body and fat mass showed a housing condition×reproductive group interaction: the challenge condition increased body and fat mass in both groups of non-reproductive males, but breeding males were unaffected. Males housed under the physical and energetic challenge had higher blood lipid content, lower maximal aerobic capacity and related traits (hematocrit and relative triceps surae mass), increased pain sensitivity and increased number of fecal boli excreted during tail-suspension tests (a measure of anxiety), compared with controls. Thus, our physical and energetic challenge paradigm altered metabolism, morphology and behavior, but these effects were largely unaffected by reproductive condition.

Paternal Care in Biparental Rodents: Intra- and Inter-individual Variation.

Parental care by fathers, although rare among mmmals, can be essential for the survival and normal development of offspring in biparental species. A growing body of research on biparental rodents has identified several developmental and experiential influences on paternal responsiveness. Some of these factors, such as pubertal maturation, interactions with pups, and cues from a pregnant mate, contribute to pronounced changes in paternal responsiveness across the course of the lifetime in individual males. Others, particularly intrauterine position during gestation and parental care received during postnatal development, can have long-term effects on paternal behavior and contribute to stable differences among individuals within a species. Focusing on five well-studied, biparental rodent species, we review the developmental and experiential factors that have been shown to influence paternal responsiveness, and consider their roles in generating both intra- and inter-individual variation. We also review hormones and neuropeptides that have been shown to modulate paternal care and discuss their potential contributions to behavioral differences within and between males. Finally, we discuss the possibility that vasopressinergic and possibly oxytocinergic signaling within the brain, modulated by gonadal steroid hormones, may represent the "final common pathway" mediating effects of developmental and experiential variables on intra- and inter-individual variation in paternal care.

Metabolic and affective consequences of fatherhood in male California mice.

Physiological and affective condition can be modulated by the social environment and parental state in mammals. However, in species in which males assist with rearing offspring, the metabolic and affective effects of pair bonding and fatherhood on males have rarely been explored. In this study we tested the hypothesis that fathers, like mothers, experience energetic costs as well as behavioral and affective changes (e.g., depression, anxiety) associated with parenthood. We tested this hypothesis in the monogamous, biparental California mouse (Peromyscus californicus). Food intake, blood glucose and lipid levels, blood insulin and leptin levels, body composition, pain sensitivity, and depression-like behavior were compared in males from three reproductive groups: virgin males (VM, housed with another male), non-breeding males (NB, housed with a tubally ligated female), and breeding males (BM, housed with a female and their first litter). We found statistically significant (P<0.007, when modified for Adaptive False Discovery Rate) or nominally significant (0.007

Consequences of Fatherhood in the Biparental California Mouse (Peromyscus californicus): Locomotor Performance, Metabolic Rate, and Organ Masses.

Although effects of motherhood on mothers have been well documented in mammals, the effects of fatherhood on fathers are not well known. We evaluated effects of being a father on key metabolic and performance measures in the California mouse, Peromyscus californicus. California mice are genetically monogamous in the wild, and fathers show similar parental behavior to mothers, with the exception of lactation. To investigate the impact of fatherhood on fathers, focal males were paired with an intact female (breeding males), a tubally ligated female (nonbreeding males), or another male (virgins). Starting 3-5 d after the birth of each breeding pair's first litter, males were tested for locomotor performance (maximum sprint speed, treadmill endurance), basal metabolic rate (BMR), and maximum oxygen consumption ([Formula: see text]). At the end of the 11-d test period, mice were euthanized, hematocrit was determined, and organs were weighed. Speed, endurance, and [Formula: see text] were significantly repeatable between two replicate measurement days but did not differ among groups, nor did BMR. Breeding males had significantly larger hind limb muscles than did nonbreeding males, whereas virgin males had heavier subcutaneous fat pads than did nonbreeding and breeding males. Several correlations were observed at the level of individual variation (residuals from ANCOVA models), including positive correlations for endurance with [Formula: see text], [Formula: see text] with testes mass, and some of the digestion-related organs with each other. These results indicate that fatherhood may not have pronounced performance, metabolic, or morphological effects on fathers, at least under standard laboratory conditions and across a single breeding cycle.