Exceptional longevity in female Rottweiler dogs is not encumbered by investment in reproduction

Abstract

To better understand the potential trade-off between female reproductive investment and longevity in an emerging model of human healthspan, we studied pet dogs to determine whether intensity of reproduction (total number of offspring) encumbered the likelihood of exceptional longevity. This hypothesis was tested by collecting and analyzing lifetime medical histories, including complete reproductive histories, for a cohort of canine "centenarians"--exceptionally long-lived Rottweiler dogs that lived more than 30% longer than the breed's average life expectancy. Reproductive intensity (number of litters, total number of pups) and tempo of reproductive effort (age at first reproduction, mean interbirth interval, age at last reproduction) in 78 exceptionally long-lived female Rottweilers (>13 years old) were compared to a cohort of 97 female Rottweilers that had usual longevity (age at death 8.0-10.75 years). We found no evidence that a mother's physiological investment in offspring was associated with disadvantaged longevity. Instead, similar to some studies in women, our data showed an inverted U-shaped trend, suggesting that moderate investment in reproduction may promote longevity. Late reproductive success, a much-studied surrogate of maternal fitness in women, was not a strong predictor of longevity in this canine cohort. Instead, independent of reproductive investment, the duration of lifetime ovary exposure was significantly associated with highly successful aging. Our results from exceptionally long-lived pet dogs provide rationale for further investigative efforts to understand the ovary-sensitive biological factors that promote healthy longevity in women and pet dogs.

Fig. 1

Increasing intensity of reproduction (total number of pups) does not diminish the likelihood of exceptional longevity in female Rottweiler dogs. (Ovary exposure in the lowest, middle, and highest groups was 6.8, 6.1, and 7.3 years, respectively. Number of female dogs in each group was 23, 24, and 21.) a Unadjusted odds ratios; *p = 0.10 compared to lowest number of pups (reference group). The p value for comparison of highest and lowest group is p = 0.28 and between highest and middle group is p = 0.59. b Adjusted odds ratios (adjusted for ovary exposure, height). The p value for comparison of middle and highest with lowest are p = 0.18 and p = 0.37, respectively; between highest and middle groups is p = 0.46. The directionality of the odds ratios (OR > 1.0) calculated by logistic regression indicates there is no apparent longevity cost to increased reproductive effort in this study population

Fig. 2

Intensity of reproduction (total number of pups) and likelihood of cancer mortality in female Rottweiler dogs. (Ovary exposure in the lowest, middle, and highest groups was 6.8, 6.1, and 7.3 years, respectively. Number of female dogs in each group was 23, 24, and 21.) Odds ratios calculated by logistic regression are adjusted for ovary exposure and mother with exceptional longevity. The p value for comparison of middle and highest with lowest are p = 0.46 and p = 0.60, respectively; between highest and middle groups, it is p = 0.88)

Fig. 3

Lifetime ovary exposure and likelihood of exceptional longevity in 104 female Rottweiler dogs without offspring (nulliparous). (Number of female dogs in each group was 51 and 53.) *p = 0.04 compared to shortest duration of ovary exposure (reference group)