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Vocal learning in some songbird species begins in the egg and these songbird embryos can discriminate the sounds of different birds. Here, we test if prenatal sound discrimination positively correlates with song complexity in the Superb Fairy-wren Malurus cyaneus. Conclusions Prenatal sound discrimination strength was positively related to vocal complexity later in life. From previous research, we know that individuals with greater learned vocal complexity may have higher fitness.
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Vocal learning in some songbird species begins in the egg and these songbird embryos can discriminate the sounds of different birds. Here, we test if prenatal sound discrimination positively correlates with song complexity in the Superb Fairy-wren Malurus cyaneus.
Conclusions Prenatal sound discrimination strength was positively related to vocal complexity later in life. From previous research, we know that individuals with greater learned vocal complexity may have higher fitness.
Therefore, characterizing the causes of prenatal sound discrimination can inform our understanding of fitness trajectories when phenotypes are shaped by learned cross-generational experience. Future research should explore causes of variance in prenatal sound discrimination. Background Songbirds are an excellent model system to study vocal learning because the structure and function of vocal learning can be tested across life stages. Using non-terminal sampling methods, neural response to song has been studied in songbirds [ 1 ], thereby allowing researchers to measure sound discrimination during the sensory and sensorimotor phases of vocal learning.
Several key insights have emerged: In studies into songbird auditory discrimination, there was high individual repeatability in learning speed across sound discrimination tasks [ 3 ]. Given recent evidence that some songbird embryos can discriminate sound [ 4 , 5 ], we were interested in whether prenatal sound discrimination can predict vocal repertoire size later in life. This prediction is congruent with what is currently known about the role of sound discrimination for vocal learning, but extends the temporal window of the sensory phase and when auditory memory and sound discrimination could occur.
Fairy-wren Malurus spp. Hatchlings with higher vocal copy accuracy of the learned begging call were fed more by the attending parents [ 7 ] and were less likely to be mistaken for a brood parasitic cuckoo hatchling and abandoned [ 4 , 8 ].
Zebra Finch embryos that were experimentally exposed to incubation calls in ovo had altered developmental trajectory post-hatch, with smaller size under warmer ambient temperature and preference for warmer nest boxes as adults [ 6 ]. Maternal effects can significantly alter the developmental trajectory of offspring [ 9 , 10 ]. Much remains to be learned about how female in-nest vocalization behavior during incubation could be a form of maternal effect that may influence offspring phenotype [ 11 ].
Prenatal exposure to incubation calls from attending females may have consequences for adult song learning [ 12 ]. For example, Red-backed Fairy-wrens M. In the Zebra Finch, male embryos experimentally exposed to incubation calls from unrelated adults produced song with more non-paternal syllables and were more likely to approach females as adults [ 13 ], pointing to an effect of prenatal vocal experience on post-hatch social behavior.
Whether an embryo can develop an auditory memory that would shape a learned vocalization during a subsequent sensorimotor phase is not known. What is known is that, similar to humans, some songbird embryos have prenatal sound learning. For example, Superb Fairy-wren M. Compared with northern hemisphere songbirds, Superb Fairy-wrens learn complex adult song relatively early in life.
We have previously interpreted the shared song repertoire of the sibling fairy-wrens as a familect that could function to reduce inbreeding via kin recognition in this long-lived sedentary species [ 14 ]. But ontogenetic mechanisms underpinning such early vocal learning of a familect remain unknown.
The 58 embryos initially lowered their heart rate baseline vs H1 to repeated exposure of 6 calls of the same female paired t-test: During the subsequent dishabituation test phase, embryos were exposed to novel stimuli 6 incubation calls of a different female Fig. The data are calculated as the difference in average HR during D minus H3 and are shown per egg age day 11, 12, 13 of incubation.
We scored HR from the digital heart rate monitor during experimental trials. A larger negative HR value was interpreted as a stronger dishabituation response sound discrimination score Full size image We compared the dishabituation response in relation to egg age day 11 to 13 of the incubation phase. Specifically, we tested for an effect of embryo age on the magnitude of the change in heart rate during exposure to a novel sound stimulus after the habituation phase.
Therefore, we included egg age as a covariate in all subsequent analyses involving sound discrimination score. This parental vocal complexity was comparable between natural and cross-fostered nests t-test: At natural nests, fledglings produced song with 8. At cross-fostered nests, fledglings produced song with 8. We compared fledgling song complexity number of vocal elements against the prenatal habituation and dishabituation sound discrimination response and parental song complexity number of vocal elements.
Better prenatal sound discrimination and increased parental song complexity predicted increased fledgling song complexity multiple regression: Fledgling acquisition of parental song elements was also influenced by prenatal performance: Data are shown for 18 field nests 12 unmanipulated nests with genetic parents, 6 cross-fostered nests with foster parents Full size image Discussion Nests with stronger prenatal sound discrimination produced fledglings with more complex song that also had a greater percentage of parental vocal elements in their song.
Fledglings had greater song complexity if their genetic and foster parents had greater song complexity. We likely underestimated the vocal repertoire of fledglings given that our analysis of vocal complexity was based on 3—5 song recordings per individual.
We note that the maximum total parental vocal repertoire 14 different element types between the adult pair may exceed what a single individual can retain, and hence also acknowledge that fledglings may prune their repertoire across the first year [ 18 ]. We fully acknowledge the limitations of the field study to draw firm conclusions. A controlled laboratory study could rear embryos with and without song exposure to elucidate the causal role if any of prenatal sound exposure for song learning.
Embryos varied in the magnitude of the dishabituation response. How sound exposure could affect development in songbirds is an emerging area of research.
The precocial chicken is a long-standing model system for the study of avian hearing, including embryonic audition [ 20 ]. In contrast, at hatch, an altricial songbird is considered to be developmentally equivalent to a half-way developed precocial hatchling [ 21 , 22 ], which raises evolutionary developmental questions about neural structures that underpin vocal learning and developmental rates across taxa.
In the altricial Zebra Finch, the model system for song learning [ 23 ], no published study to date has examined in ovo response to sound directly, but embryos exposed to prenatal noise their parents were also exposed to noise had higher mortality, indicating some capacity to be impacted by prenatal sound [ 24 ]. Postnatal response to prenatal incubation calling was nevertheless found in Zebra Finch nestlings: Much remains to be discovered about the role of early sensory exposure for the development of neural networks, anatomical structures and biochemical pathways for processing sensory input.
We predict there will be lineage-specific differences in the ontogeny of sound perception and vocal production that could influence rates of evolution in vocal learning lineages [ 27 , 28 , 29 , 30 , 31 ]. It is possible that the prenatal sound discrimination forms part of the species-specific innate template for song learning. Nature-nurture perspectives to explore possible causes and consequences of prenatal sound experience generate exciting evolutionary questions about the ontogeny of auditory memory and vocal learning [ 32 , 33 ].
For example, isolation-reared Zebra Finches preferred conspecific song [ 34 ] and juveniles tutored by isolate-reared males with atypical song tended to revert to wild-type song after three to four generations [ 35 ], thereby demonstrating different lines of evidence for genetic predisposition for species-specific song. In addition to genetic predisposition for song type, other studies have revealed how experience can influence genetic variation and shape interindividual differences in learned song [ 36 ].
There is much to be discovered about factors that govern prenatal sound discrimination, including effects of instructive vocal experience before hatching, and how early sound experience can shape preference and behavior that directs vocal learning later in life. Conclusions Field studies are vital to inform the design of experimental research in behavioral ecology. Early sound discrimination capacity may be innate or it may be enhanced through exposure to prenatal vocal tutors.
In a vocal learning songbird, prenatal sound discrimination and parental song complexity may predispose individuals to change behaviors relevant for song learning. The study was conducted at two study sites in South Australia: Field studies are vital to maintain the biological relevance of questions e. To cross-foster nest contents, we swapped entire clutches of eggs on day d 5 or d 6 after the onset of incubation between two nests with same egg age.
All tests involving prenatal sound exposure were done on d 11 to d 13 of the incubation phase. We describe each method and variable below, but provide a summary overview of sample size here, noting that sample size was impacted by predation at nests:
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Could prenatal sound discrimination predict vocal complexity later in life?
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