Ground squirrels hibernate through puberty

Abstract

Comparative physiologists love studying trade-offs, the compromises that animals make to balance competing needs in challenging environments. If there is barely enough food to survive, then extracurriculars such as growth, reproduction or even routine activity will take a back seat. Thirteen-lined ground squirrels take this trade-off to the extreme, hibernating through much of the year in a coma-like state known as torpor. After observing several young squirrels become fathers almost immediately upon emerging from torpor, Rafael Dai Pra from Yale University, USA, and colleagues hypothesized that juvenile squirrels became sexually mature during their maiden hibernation season. Recently published in Current Biology, their research used a combination of endocrinology and neurophysiology to show that thirteen-lined ground squirrels approach trade-offs a little bit differently than other animals.Dai Pra and colleagues monitored juvenile males going through their first ever hibernation season and took tissue samples to track how their reproductive system changed over time. Not surprisingly for animals that do not eat or drink, the squirrels lost 48% of their body mass during hibernation, largely from the depletion of fat reserves. Their body temperature plummeted to a chilly 4°C, only warming for brief periods of interbout arousal when the squirrels briefly regained consciousness. Losing mass, cold and inactive, hibernating squirrels clearly experienced a profound negative energy imbalance akin to starvation.Starved and cold mammals rarely reproduce, as poor conditions inhibit the release of sex hormones, thereby delaying sexual maturation and activity. Not so for the squirrels. The serum levels of luteinizing hormone, which tells the testicles to make testosterone, and testosterone itself climbed over the hibernation period. Changes in the young squirrels’ brains caused these hormonal changes: the hypothalamus of hibernating squirrels had far more cells expressing kisspeptin, a protein that triggers the release of luteinizing hormone from the pituitary gland, compared with active squirrels. Swimming in sex hormones, the young hibernating males’ reproductive systems kicked into high gear: their testicles doubled in size between the time that they entered hibernation and the time when they emerged.With clear evidence that thirteen-lined ground squirrels completed puberty during their first hibernation, the researchers turned their attention to understanding how they co-ordinated this process without light, food or warmth to stimulate them. To do this, they brought in a new set of juvenile males, this time holding them in comfortable conditions to prevent them from hibernating and monitored their body mass, fat stores and hormones, like the hibernating squirrels. The non-hibernating squirrels experienced similar changes in testosterone and testicle size as hibernators. They also gained lean mass and lost fat, both of which consistent with the effects of elevated testosterone. This means that thirteen-lined ground squirrels are capable of going through puberty regardless of whether they are fed or starving, cold or warm, hibernating or active.As a species, thirteen-lined ground squirrels live an extreme life, having as little as 5 months to get all of their business done, such as mating, digging burrows and fattening up, before waiting out the rest of the year in suspended animation. Motivated by this tight deadline, they have figured out a way to prioritize reproduction when resources are scarce and, in doing so, show us that trade-offs are not as predictable as we might think.