Reproductive capability is associated with lifespan and cause of death in companion dogs

Abstract

Reproduction is a risky affair; a lifespan cost of maintaining reproductive capability, and of reproduction itself, has been demonstrated in a wide range of animal species. However, little is understood about the mechanisms underlying this relationship. Most cost-of-reproduction studies simply ask how reproduction influences age at death, but are blind to the subjects' actual causes of death. Lifespan is a composite variable of myriad causes of death and it has not been clear whether the consequences of reproduction or of reproductive capability influence all causes of death equally. To address this gap in understanding, we compared causes of death among over 40,000 sterilized and reproductively intact domestic dogs, Canis lupus familiaris. We found that sterilization was strongly associated with an increase in lifespan, and while it decreased risk of death from some causes, such as infectious disease, it actually increased risk of death from others, such as cancer. These findings suggest that to understand how reproduction affects lifespan, a shift in research focus is needed. Beyond the impact of reproduction on when individuals die, we must investigate its impact on why individuals die, and subsequently must identify the mechanisms by which these causes of death are influenced by the physiology associated with reproductive capability. Such an approach may also clarify the effects of reproduction on lifespan in people.

Figure 1. Effect of sterilization on longevity and diagnoses.

(A) Kaplan-Meier plots of longevity for males (left) and females (right). Blue lines indicate sterilized dogs and red lines indicate intact dogs. (B) Common log-odds ratios with 95% confidence intervals (CI) for pathophysiological processes (PP). Height of each bar indicates the relative frequency of each PP among all deaths. (C) Effects of sterilization on specific neoplastic diagnoses, showing common log odds ratios and 95% CI. Height of each bar indicates fraction of individuals with this diagnosis at the time of death. Transitional CC – transitional cell carcinoma; Squamous CC – squamous cell carcinoma. All cancers significant at P<0.01 except prostate cancer, squamous cell carcinoma and melanoma (P>0.05). (D) As in Figure 1C, but for specific infectious disease diagnoses. All infectious diseases significant at P<0.01 except blastomycosis (P>0.4).

Figure 2. Breed specific causes of mortality.

Effects of sterilization on the 24 pure breeds that appear most frequently in our dataset (minimum sample size = 319, median sample size = 517). Bars indicate 95% CI. Colors of odds ratio bars indicate size of the breed (red-small [up to 10 kg], blue-medium [10.1–25 kg], green-large [25.1–40 kg], yellow-giant [>40 kg]). Breed abbreviations are shown (LA: Lhasa Apso, SCT: Scottish Terrier, SHT: Shih Tzu, YT: Yorkshire Terrier, TP: Toy Poodle, DACH: Dachshund, MS: Miniature Schnauzer, MP: Miniature Poodle, BH: Basset Hound, BEA: Beagle, ESS: English Springer Spaniel, COLL: Collie, ACS: American Cocker Spaniel, SH: Siberian Husky, IS: Irish Setter, SP: Standard Poodle, BOX: Boxer, SS: Shetland Sheepdog, DP: Doberman Pinscher, GS: German Shepherd, LR: Labrador Retriever, GR: Golden Retriever, GD: Great Dane, ROT: Rottweiler).