Beneath the fluffy backsides of Valerie Robson's two male golden retrievers is an unusual sight: intact anatomy. Neither dog is neutered.
This presents occasional challenges. Astro and Rumble are barred from most doggy day-cares, and many boarding kennels won't take them. But although Robson has no intention of breeding the dogs, she says she has no regrets. Research that suggests neutering could be linked to cancers and joint disorders persuaded her that skipping sterilization is best for her pets.
"Sometimes people notice," said Robson, a county government employee in Conifer, Colo. "I just explain that we chose to do this for health and wellness, and he's a good boy, and it's never been an issue."
"Intact" dogs were the norm for a long time, and a litter of puppies was often part of the deal. But in the 1970s, when overflowing animal shelters were euthanizing millions of homeless dogs annually, spaying and neutering puppies - procedures that involve removing ovaries or testicles - became the dogma in the United States.
It still is: Surveys indicate a large majority of pet dogs are fixed, and 31 states and the District require that pets adopted from shelters or rescues be sterilized. The surgeries simplify pet ownership by preventing females from going into heat and, some believe, by improving dog behavior, though experts say that is not clearly supported by research.
But the common wisdom has been complicated in recent years amid widening evidence connecting spaying and neutering to health problems in dogs. The findings are stronger for certain breeds and large dogs, and age of neutering plays a role. But the research is causing some owners and veterinarians to question the long-held tenet that fixing puppies - or fixing, period - is a necessary part of responsible pet ownership.
"We owe it to our dogs to have a much larger conversation about spay and neuter," said Missy Simpson, a veterinary epidemiologist with the Morris Animal Foundation, a charity that funds animal health research. "It's nuanced, and there isn't a great one-size-fits-all recommendation for every dog."
Simpson was lead author of a recent paper on about 2,800 golden retrievers enrolled in a lifetime study, which found that those spayed or neutered were more likely to be overweight or obese. The study also found that dogs fixed before they were 6 months old had much higher rates of orthopedic injuries, and that keeping dogs lean didn't prevent those injuries.
The research has sparked controversy in the veterinary and shelter worlds, in part because widespread spaying and neutering are credited with helping fuel a dramatic decline in euthanasia. The American Society for the Prevention of Cruelty to Animals, which says about 670,000 dogs are killed in shelters each year, supports "early-age" sterilization.
"The question on a bigger level is to what extent are we sacrificing some bits of welfare for an individual animal for the welfare of the species?" said Stephen Zawistowski, science adviser emeritus at the ASPCA. "The fact that we can actually have the conversation is a sign that we've made such enormous progress."
Spaying and neutering do have some clear health benefits for dogs. Testicular and ovarian cancers are moot, and there's evidence that spaying lowers the risk of mammary cancer and uterine infections. Fixed dogs also live longer on average.
But researchers say the reproductive hormones controlled by the removed sex organs have important systemic roles. They influence muscle mass and tendon and ligament strength, and they tell bones when to stop growing. "Without those hormones, your body might just not be as robust," Simpson said.
The recent debate over spaying and neutering flared in 2013, when a study from the University of California at Davis reported higher rates of hip dysplasia, cranial cruciate ligament tears and certain cancers among desexed golden retrievers - especially those neutered early, defined as before 1 year of age. The paper caused "quite a bit of controversy" among critics who "accused us of, you know, driving overpopulation of animals," said author Benjamin Hart, a professor emeritus at Davis's vet school.
Hart and his colleagues later found higher rates of joint disorders, but not cancers, among Labrador retrievers and German shepherds that were neutered early. Their latest study, which is not yet published, examined 35 breeds and mutts and detected no associations between desexing and cancers or joint disorders in small dogs. But it found much greater rates of joint disorders among nearly all large dogs sterilized early, Hart said.
"Dogs vary tremendously in their physiology, their anatomy. It's not surprising they would vary in these other things," Hart said. "It is complicated. That's why people need to talk it over with their veterinarian."
The American Veterinary Medical Association agrees, saying decisions should be made on a case-by-case basis.
Michael Petty, a veterinarian in Canton, Michigan, used to give the standard guidance: Spay or neuter at 6 months. But when he began seeing lots of ruptured cruciate ligaments among dogs neutered young, he wondered whether there was a connection. Based on research that has come out since, for the past decade or so, he has advised clients to hold off on sterilization until dogs reach puberty.
It's easier to spay a puppy than an adult dog, Petty said. "But are we causing a problem down the road? We really have to say: First, do no harm."
Spaying and neutering are much less common in Europe. Alexandra Horowitz, a dog cognition researcher at Barnard College, says in her new book, "Our Dogs, Ourselves," that their widespread use here is an indictment of Americans' too-casual approach to pet ownership.
"We're asking dogs to take on the responsibility for our actions," Horowitz said in an interview - and, she added, for our squeamishness. "Our culture is so caught up in the notion that our dogs shouldn't be sexual, and spay-neuter kind of feeds into that."
Owning intact dogs can be less convenient. Females bleed when in heat, and males are more prone to urine-marking.
Robson, the owner of Rumble and Astro, said her dogs don't do that. Her first five dogs were rescues, and all were fixed before she took them in. But when she purchased Astro, his breeder had a condition: Don't neuter until he's 2. By then, Astro's vet - citing research on neutered golden retrievers and cancer - suggested that she leave him intact.
Astro is "so mellow," Robson said, that she agreed. It helps that they live on a lot of land in the Denver foothills, far from other dogs.
"As an owner, you have to be comfortable with your ability to supervise them and to make sure they're not going to run off and do something stupid and get caught with a girl," said Robson, whose younger dog, Rumble, is enrolled in the golden retriever lifetime study.
Sherri Wilson, an accountant in Grand Junction, Colorado, had a similar experience. The breeder of her 5-year-old golden retriever, Bailey, asked that she wait until he was 18 months old to neuter him.
"We got to 18 months, and it was like, why would we do it? He had no behavior problems, no aggression," she said. "We couldn't see a reason to do it, and we could see several reasons not to do it."
People active in dog sports pay close attention to research on joint problems, and many now choose not to spay or neuter, said Wendy Garvin, a dog trainer in Riverton, Utah. Her five intact pooches do agility, dock-diving and other sports.
Four years ago, Garvin started a Facebook group that offers advice on managing dogs that aren't spayed or neutered. Owners need to know how to keep males and females apart when necessary, she said, and how to recognize when females are coming into heat (in her house, she said, it's when "the boys get stupid," doing things like licking the females' privates and humping).
"There are people who would love to sell you a bundle of roses with it," she said. "I would rather be realistic about it."
Garvin said the Facebook group grows by about 20 to 30 people each month, many ordinary pet owners. In some cases, she recommends that they opt for vasectomies or hysterectomies for their dogs - procedures that prevent reproduction but spare hormones. A small but growing number of veterinarians perform them.
"People are pretty capable if they take ownership of their responsibility," she said. But, she added, "none of us want to see more unwanted puppies."