Puppy whines mediate maternal behavior in domestic dogs

Abstract

In mammals, offspring vocalizations typically encode information about identity and body condition, allowing parents to limit alloparenting and adjust care. But how do these vocalizations mediate parental behavior in species faced with the problem of rearing not one, but multiple offspring, such as domestic dogs? Comprehensive acoustic analyses of 4,400 whines recorded from 220 Beagle puppies in 40 litters revealed litter and individual (within litter) differences in call acoustic structure. By then playing resynthesized whines to mothers, we showed that they provided more care to their litters, and were more likely to carry the emitting loudspeaker to the nest, in response to whine variants derived from their own puppies than from strangers. Importantly, care provisioning was attenuated by experimentally moving the fundamental frequency (f_o, perceived as pitch) of their own puppies' whines outside their litter-specific range. Within most litters, we found a negative relationship between puppies' whine f_o and body weight. Consistent with this, playbacks showed that maternal care was stronger in response to high-pitched whine variants simulating relatively small offspring within their own litter's range compared to lower-pitched variants simulating larger offspring. We thus show that maternal care in a litter-rearing species relies on a dual assessment of offspring identity and condition, largely based on level-specific inter- and intra-litter variation in offspring call f_o. This dual encoding system highlights how, even in a long-domesticated species, vocalizations reflect selective pressures to meet species-specific needs. Comparative work should now investigate whether similar communication systems have convergently evolved in other litter-rearing species.

Keywords: domestic dog; individual discrimination; litter-rearing mammals; parental care; vocal communication.

Fig. 1.

Acoustic analyses and preparation of synthetic whine stimuli for playback experiments. (A) Litters have specific f_o ranges, and within most litters, individual puppy whine f_o is negatively correlated with body weight, as illustrated with the pink solid lines. Positive or null relationships between puppy whine f_o and body weight are indicated with dashed black lines. Each dot corresponds to a puppy, and each line represents the slope of the correlation within a litter. (B) To test the extent to which mothers use f_o to discriminate their own puppies from stranger puppies, we created synthetic whine variants from stranger or own-puppy natural whine exemplars with a f_o falling inside the tested mother’s litter frequency range (litter-typical, central spectrograms in purple range) or with a f_o falling outside the litter range (litter-atypical, upper and lower spectrograms in blue range). To test the extent to which mothers use f_o to assess the body weight of puppies, we also created variants where the f_o was set to simulate either a relatively small puppy (relatively high f_o within litter range) or large puppy (relatively low f_o within litter range) for the given tested litter.

Fig. 2.

The fundamental frequency f_o of puppy whines predicts maternal care responses to playbacks of her offspring. Maternal responses are quantified using a behavioral index (Table 1 and Materials and Methods). Each dot (fitted value) represents a single playback experiment. The dot shape indicates the mother’s identity, and the dot color indicates whether the tested mother was presented with whines characterized by a f_o manipulated to fall inside (purple) or outside (blue) their litter range. The black solid lines correspond to the regression trendlines and the gray shaded areas to the 95% CIs. (A) Mothers provided more care in response to acoustic variants derived from their own puppies’ whines where f_o was manipulated to fall inside their litter f_o range (litter-typical) than to those where f_o was manipulated to fall outside the litter f_o range (litter atypical). This response was not observed when the broadcasted whine variants were derived from the whines of stranger puppies. (B) Mothers provided more care in response to playbacks of their own puppies when f_o was manipulated to be relatively high (mimicking relatively small puppies for their litter) compared to those when f_o was manipulated to be relatively low (mimicking relatively large puppies for their litter). The level of maternal care was not affected by f_o manipulations in stranger puppy whines.