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Biology subjects

Maney, D. L.

Publications and source records attributed to Maney, D. L..

7 recordsLinked to original sources

Opposing behavioral roles for a single gene in a species with a supergene polymorphism

Behavioral trade-offs, such as between territorial aggression and parental care, require coordination among neural and genetic mechanisms that influence opposing phenotypes. In some systems, including the white-throated sparrow, this coordination has been proposed to be mediated in part by chromosomal inversions that bind together multiple genes associated with alternative strategies. Here, we demonstrate that opposing components of a life-history trade-off can be linked, via alternative alleles inside a chromosomal rearrangement, to a single pleiotropic gene. In white-throated sparrows, a species with polymorphic aggressive and parental behavior, the gene encoding the neuromodulator vasoactive intestinal peptide (VIP) lies within an inversion-based supergene. Working with a free-living population, we found that VIP expression in a pro-aggression cell population in the anterior hypothalamus positively predicted territorial singing, whereas expression in a pro-parental cell population in the infundibular nucleus positively predicted parental provisioning. Expression in these two regions was negatively correlated, consistent with opposing behavioral roles. Allele-specific analyses revealed stronger expression bias toward the supergene-associated allele in the anterior hypothalamus than in the infundibular nucleus. These findings suggest that chromosomal inversions can support opposing behavioral phenotypes not only by linking multiple genes, but also by driving regulatory divergence of individual genes that organize behavioral trade-offs.

neuroscience↗

The 'sex-specific effect:' Evaluating analytical approaches to sex-dependence in the behavioral and brain sciences

Detecting a sex difference in response to a treatment or intervention, often reported as a "sex-specific effect," requires statistical comparison of the response across sex. Here, we investigated analytical approaches used to test for such effects in the behavioral and brain sciences. Of 200 recent articles containing terms such as sex-specific or gender-dependent in their titles, only 24% presented appropriate evidence supporting the claim: the effect was compared statistically across sex and results consistent with the claim were reported. In most articles (58%), no test was conducted that could have supported the title claim. Only 15% of studies on non-human animals supported the claim with appropriate evidence, which was significantly less frequently than studies on human participants (34%; p = 0.002). The use of appropriate analytical approaches was unrelated to journal rank or the citation impact of the article. We conclude that claims of sex/gender-dependent effects in the behavioral and brain sciences are only infrequently supported by appropriate evidence.

neuroscience↗

Dynamic molecular evolution of a supergene with suppressed recombination in white-throated sparrows

In white throated sparrows, two alternative morphs differing in plumage and behavior segregate with a large chromosomal rearrangement. As with sex chromosomes such as the mammalian Y, the rearranged version of chromosome two (ZAL2m) is in a near-constant state of heterozygosity, offering opportunities to investigate both degenerative and selective processes during the early evolutionary stages of supergenes. Here, we generated, synthesized, and analyzed extensive genome-scale data to better understand the forces shaping the evolution of the ZAL2m chromosome in this species. We found that features of ZAL2m are consistent with substantially reduced recombination and low levels of degeneration. We also found evidence that selective sweeps took place both on ZAL2m and its standard counterpart, ZAL2, after the rearrangement event. Signatures of positive selection were associated with allelic bias in gene expression, suggesting that antagonistic selection has operated on gene regulation. Finally, we discovered a region exhibiting two long-range haplotypes inside the rearrangement on ZAL2m. These two haplotypes appear to have been maintained by balancing selection, retaining genetic diversity within the supergene. Together, our analyses illuminate mechanisms contributing to the evolution of a young chromosomal polymorphism, revealing complex selective processes acting concurrently with genetic degeneration to drive the evolution of supergenes.

evolutionary biology↗

Oxytocin receptor antagonism during song tutoring in zebra finches reduces preference for and learning of the tutor's song

In species with vocal learning, acquiring species-typical vocalizations relies on early social orienting. In zebra finches (Taeniopygia guttata), for example, learning song requires dynamic social interactions with a "tutor" during an early sensitive period. The oxytocin system plays a central role in social orienting across species, yet it is unknown whether this system participates in the attentional and motivational processes that support vocal learning. Here, we tested whether blocking oxytocin receptors during exposure to tutors would impact learning from those tutors. Juvenile, song-naive males were each tutored by two unfamiliar adults. During exposure to one tutor, juveniles were treated with oxytocin receptor antagonist (OTA) and during exposure to the other, saline (control). We found that OTA significantly reduced behaviors associated with approach and attention during tutoring sessions. Next, using an operant assay in which exposure to the two songs was balanced, we found that the juveniles preferred the control song over the OTA song. The developmental trajectory of preference for the control song resembled the pattern shown by father-reared birds choosing to hear their fathers song. Finally, the adult songs of the tutored birds more closely resembled control song than OTA song. The magnitude of this difference was significantly predicted by the early preference for the control song. Overall, oxytocin antagonism during exposure to a tutor seemed to bias juveniles against that tutor and his song. Our results suggest that oxytocin receptors play a role in socially-guided vocal learning in zebra finches, perhaps by affecting attention and motivation during tutoring.

animal behavior and cognition↗

Song preferences predict the quality of vocal learning in zebra finches

In songbirds, learning to sing is a highly social process that likely involves social reward. Here, we hypothesized that the degree to which a juvenile songbird learns a song depends on the degree to which it finds that song rewarding to hear during vocal development. We tested this hypothesis by measuring song preferences in young birds during song learning and then analyzing their adult songs. Song preferences were measured in an operant key-pressing assay. Juvenile male zebra finches (Taeniopygia guttata) had access to two keys, each of which was associated with a higher likelihood of playing the song of their father or that of another familiar adult ("neighbor"). To minimize the effects of exposure on learning, we implemented a reinforcement schedule that allowed us to detect preferences while balancing exposure to each song. On average, the juveniles significantly preferred the fathers song early during song learning, before they were themselves singing. At around post-hatch day 60, their preference shifted to the neighbors song. At the end of the song learning period, we recorded the juveniles songs and compared them to the fathers and the neighbors song. All of the birds copied fathers song. The accuracy with which the fathers song was imitated was positively correlated with the peak strength of the preference for the fathers song during the sensitive period. Our results show that preference for a social stimulus, in this case a vocalization, predicted social learning during development.

animal behavior and cognition↗

Reporting and Misreporting of Sex Differences in the Biological Sciences

As part of an initiative to improve rigor and reproducibility in biomedical research, the U. S. National Institutes of Health now requires the consideration of sex as a biological variable in preclinical studies. This new policy has been interpreted by some as a call to compare males and females with each other. Researchers testing for sex differences may not be trained to do so, however, increasing risk for misinterpretation of results. Using a list of recently published articles curated by Woitowich et al. (eLife, 2020; 9:e56344), we examined reports of sex differences and non-differences across nine biological disciplines. Sex differences were claimed in the majority of the 147 articles we analyzed; however, statistical evidence supporting those differences was often missing. For example, when a sex-specific effect of a manipulation was claimed, authors usually had not tested statistically whether females and males responded differently. Thus, sex-specific effects may be over-reported. In contrast, we also encountered practices that could mask sex differences, such as pooling the sexes without first testing for a difference. Our findings support the need for continuing efforts to train researchers how to test for and report sex differences in order to promote rigor and reproducibility in biomedical research.

scientific communication and education↗

Expression of oxytocin receptors in the zebra finch brain during vocal development

Juvenile male zebra finches memorize and learn to sing the song of a male caregiver, or \"tutor\", during a complex vocal learning process. Juveniles are highly motivated to interact socially with their tutor, and these interactions are required for effective vocal learning. It is currently unknown what neurological mechanisms underlie attraction to tutors, but social motivation and affiliation in this and other species may be mediated by oxytocin and related nonapeptides. Here, we used qPCR to quantify expression of oxytocin receptor (OTR) mRNA in the lateral septum, auditory forebrain, and regions of the song control system in zebra finches throughout post-hatch development and vocal learning. We found that zebra finches express OTR mRNA in these regions from post-hatch day 5 to adulthood, encompassing the entire period of auditory and sensorimotor learning. We also mapped the binding of 125I-ornithine vasotocin, an oxytocin receptor antagonist that binds to oxytocin receptors in songbird brain, to understand the neuroanatomical distribution of oxytocin-like action during vocal development. This study provides the groundwork for the use of zebra finches as a model for understanding the mechanisms underlying social motivation and its role in vocal development.

neuroscience↗