Colony-specific dialects of naked mole-rats

doi:10.1126/science.abf7962

GSTDTAP > 气候变化

DOI	10.1126/science.abf7962
	Colony-specific dialects of naked mole-rats
	Rochelle Buffenstein
	2021-01-29
发表期刊	Science
出版年	2021
英文摘要	Oral communication is an essential component of vertebrate social living. Even so, few animals are vocal learners. Rather, in most species vocalizations are instinctive, immutable, and genetically determined. Humans, whales, and songbirds are well-known exceptions, with elaborate language learned in early life using vocal mimicry, thereby creating distinctive geographic dialects or accents. These vocalizations nevertheless retain acoustic flexibility. On page 503 of this issue, Barker et al. ([ 1 ][1]) show that unlike other rodents, the almost blind, highly social, yet xenophobic, naked mole-rat has a colony-specific greeting—the soft chirp—that is learned in early life and facilitates recognition of colony members and thereby helps maintain colony cohesiveness. This soft-chirp signature appears to be modulated by the matriarch, or “queen.” Should she die, or new colonies form by fission or outbreeding, after a period of acoustic variability the dialect once again becomes fixed and specific to the colony when a new queen is established. Naked mole-rats are eusocial, subterranean rodents that live in socially hierarchical groups dominated by the queen. With the evolution of social living came the need to communicate effectively, thereby enabling group recognition, social organization, cooperative division of labor, and conflict avoidance. Similarly, elaborate communication systems are evident in eusocial insects—for example, the waggle dance of bees ([ 2 ][2]). Naked mole-rats, unable to rely on visual cues, have acquired a vocal repertoire ([ 3 ][3], [ 4 ][4]) that conveys considerable information about the emitters—including size and social status, as well as their intentions. As Barker et al. observed, they have a distinctive, colony-specific soft chirp that is used when animals encounter each other in their underground maze. This voice-recognizing, colony-specific dialect is analogous to human regional and ethnic accents and/or dialects. The complexity of naked mole-rat vocalizations and responses suggests sophisticated cognitive comprehensive abilities, requiring intricate neural control and coordination of vocal motor structures and breathing. Naked mole-rats are extremely xenophobic ([ 5 ][5]) and readily attack and kill animals from other colonies if they are mistakenly returned to a wrong colony in captivity ([ 6 ][6]); they likely respond similarly to intruders in the wild. This intolerance of foreign conspecifics assists in maintaining their unusual lifestyle that is heavily reliant on kin selection and altruistic behaviors (e.g., shared pickings from foraging bouts) for the needs of the entire colony. The colony-specific greeting enables mole-rats to recognize intruders immediately, and thereafter, elicit appropriate colony defenses. Alien recognition prevents colony mixing, particularly foiling foreign males from mating with the queen and reducing genetic relatedness among colony members. Such xenophobic actions are a corollary of kin selection and concomitant altruistic behavior ([ 7 ][7]). Although vocal learning is an expensive trait, colony-identifying greetings are vital for their species fitness, survival, and colony cohesion. Like human language, whale calls, and bird songs, the soft-chirp dialect appears to be learned, probably by vocal mimicry, and requires memorization of sensory inputs stored as an acoustic template and subsequently translated into template-matching vocal outputs ([ 8 ][8]). This is an astonishing feat for a rodent and is in stark contrast to the majority of mammalian vocalizations, which are innate, immutable, and genetically inherited ([ 9 ][9]). The colony-specific dialect, like that of human infants, is attained in early life by repeatedly hearing the sounds emitted by adults in the colony. Again, analogous to humans, there appears to be a critical period in which refinement of pup babbles can occur—a process requiring considerable practice to mold vocalizations until these precisely recapitulate adult sounds. Presumably, this life cycle–dependent, learned vocalization also reflects developmental changes in the anatomy of vocal and auditory tracts, as well as active sensory motor learning processes. It has been recently reported that in the wild, small colonies of naked mole-rats allegedly may invade neighboring colonies and “kidnap” young pups ([ 10 ][10]). Integrating this observation with the cross-fostering findings of Barker et al. , it is likely that these “enslaved” pups would learn the colony vocalizations of their captors. In turn, this would facilitate their acceptance into a genetically unrelated colony and thus expand its workforce by engaging them in burrow maintenance and food location, albeit at the expense of their own fitness ([ 10 ][10]). Although the colony-specific dialect is learned during the critical period of pup maturation, Barker et al. showed that dialects of fostered offspring may be slightly imperfect, suggesting that these were not accurately learned, possibly because learning may have started a little later in their life cycle. Barker et al. observed that the naked mole-rat soft-chirp signature retains acoustic flexibility. The precise dialect of the colony is greatly influenced by the matriarch, whose chirps may be critical for indicating her continued presence, dominance, and suppression of reproduction in other colony members. This raises several interesting possibilities: Does her more precise chirp constantly retune and calibrate the dialect sound architecture through active template matching? More parsimoniously, could colony members be matching their dialect to the average sound features encountered within the colony environment? In this case, could the presence of the queen serve to restrict individual variability? Regardless, these possibilities would require sophisticated neural computations for sensorimotor processing and provide a detectable vocal signal of nonconformity. Dialect nonconformity by a particular individual within the colony might be met with intracolony conspecific aggression to uphold colony stability. Only breeding males show considerable variability in the soft chirp. Although this may reflect a hormonal role in vocal plasticity, it is possible that this more varied chirp may contribute to mate selection by the queen and that she chooses the male she mates with on the basis of his beguiling voice, in much the same way that songbirds do ([ 11 ][11]). Should the queen die, colony vocalizations become less precise and the colony less cohesive, leading to dispersal or fights for reproductive dominance. Mole-rats modify their dialects when a new colony is formed, regardless of whether this is due to the rise of a new dominant female within an existing colony, colony fission, or pairing of unrelated individuals. Establishment of a new dialect distinguishes the newly formed colony as an independent, distinct social unit. Dialect plasticity highlights that memorization-based vocal learning can and does also occur in adults. Barker et al. have revealed marked similarities between the learned, and complex vocalizations of naked mole-rats, songbirds, and humans, and many intriguing questions follow. For example, do these very disparate taxa all employ the same developmental trajectory, brain mechanisms, and regulatory genes to regulate vocal learning? Clearly such evolutionary convergence in learned vocalizations offers a valuable opportunity to decode the shared mechanistic and neurogenetic basis of vocal learning and get a little closer to understanding the origins of human language. 1. [↵][12]1. A. J. Barker et al ., Science 371, 503 (2021). [OpenUrl][13][Abstract/FREE Full Text][14] 2. [↵][15]1. A. B. Barron, 2. J. A. Plath , J. Exp. Biol. 220, 4339 (2017). [OpenUrl][16][Abstract/FREE Full Text][17] 3. [↵][18]1. K. Okanoya et al ., J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 204, 905 (2018). [OpenUrl][19] 4. [↵][20]1. S. Yosida, 2. K. Okanoya , Ethology 115, 823 (2009). 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领域	气候变化 ; 资源环境
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文献类型	期刊论文
条目标识符	http://119.78.100.173/C666/handle/2XK7JSWQ/314001
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Rochelle Buffenstein. Colony-specific dialects of naked mole-rats[J]. Science,2021.
APA	Rochelle Buffenstein.(2021).Colony-specific dialects of naked mole-rats.Science.
MLA	Rochelle Buffenstein."Colony-specific dialects of naked mole-rats".Science (2021).