WIKIMEDIA, RAMANon-monogamous male lab mice are not natural fathers, but they do provide parental care when housed together with their mates and pups for a few days. Now, scientists in Japan have demonstrated that when both parents are separated from the pups, the mother communicates through ultrasonic vocalisations (USVs) and odor cues to stimulate the father to provide parental care when the offspring are returned. So it seems that when the mother fears for her pups, she tells the father to get involved. The findings were published today (January 8) in Nature Communications.
“We have shown before that male mice having been fathers for 5 days are ready for pup care, while fathers with 1 day of pup experience are not,” said Günter Ehret, a neurobiologist at the University of Ulm in Germany, who was not involved in the research. “This study suggests that not only the pups stimulate the males to become caring father after 5 days of contact, [but also] that the pup’s mother signals to the father that the pups may need help.”
Haruhiro Higashida and colleagues at Kanazawa University in Japan set about trying to find out precisely what motivates male mice to become active parents by studying pup retrieval behavior. When a new mating pair is continuously housed together with the pups, sires gathered and tended to pups very infrequently for the first 3 to 5 days, but then began showing signs of parental care. If at that point they are separated from the pups for 10 minutes and co-housed with the mother, sires displayed retrieval behavior when reunited with the pups. But male mice housed alone in a new cage during pup separation did not, suggesting the cues come from the pups, the mothers, or both.
Next the researchers setup a cage with three separate but accessible chambers. Sires were removed from their families and placed in the center chamber, either alone or with their mates for 3, 5, or 10 minutes. Five pups were then placed in the left chamber. Sires that had cohabited with mates during pup separation tended to move through all chambers with equal frequency. But sires isolated alone showed a preference for the empty chamber, indicating that the mother is important in encouraging the male’s parental behavior.
To find out the nature of the mothers’ signals, the researchers first placed the mother in an open-topped clear plastic box that allowed for visual, olfactory, and auditory communication, but prevented physical contact with the males. This did not affect the fathers’ behavior. But when the mothers were placed in a box with a lid, preventing auditory and olfactory cues, the proportion of sires to display retrieval behavior dropped significantly.
Ultrasound recordings during pup separation revealed short of bursts of USVs. When the recordings were played back to sires housed alone during pup separation, 60 percent of them retrieved pups, compared to none of the sires that were played a control noise of the same frequency.
The researchers also showed that olfactory cues play a part. Exposing sires to maternal pheromones left in cages by mothers that had been separated from their pups resulted in pup retrieval in 55 percent of sires tested. When olfactory cues were combined with pre-recorded USVs, that figure rose to 67 percent. Furthermore, when sires were rendered either deaf or anosmic, pup retrieval behaviour was not diminished. But of the sires rendered both deaf and anosmic, not one displayed parental care behavior.
“The study presents remarkable results,” said Ehret. “[It] indicates that a certain type of ultrasound and/or odor of mothers increase the father’s motivation for paternal care. It seems as if the mother communicates her fear because of the loss of her children to the father to make him attentive and motivated to be a good father and carry the children back in case he finds them by accident.”
H.X Liu et al., “Displays of paternal mouse pup retrieval following communicative interaction with maternal mates,” Nature Communications, doi: 10.1038/ncomms2336, 2013